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Triclabendazole progress report, 2005–2009: an advancement of learning?

Published online by Cambridge University Press:  01 June 2009

I. Fairweather
I. Fairweather*
Affiliation:
Parasite Therapeutics Research Group, School of Biological Sciences, Medical Biology Centre, The Queen's University of Belfast, 97, Lisburn Road, BelfastBT9 7BL, Northern Ireland, UK
*
*Fax: +44 2890975877 E-mail: i.fairweather@qub.ac.uk
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Abstract

Triclabendazole (TCBZ) remains the drug of choice for treating infections of the liver fluke, Fasciola hepatica in livestock and has become the main drug used to treat human cases of the disease as well. Cases of resistance in livestock continue to be reported, suggesting that the problem is increasing. In order to address the problem, there is a need for better understanding of drug action. A ‘state-of-play’ review on different aspects of TCBZ activity was published by the present author in 2005. The main purpose of the current review is to assess what progress has been made in the past four years towards understanding the main aspects of drug activity, including drug pharmacokinetics and pharmacodynamics and an understanding of the mechanism(s) of resistance. Also, what advances have been made in identifying alternative compounds and using drug combinations to enhance TCBZ activity. Stemming from a number of in vivo studies, it has become evident that fluke isolates of differing sensitivity to TCBZ differ in some of their biological parameters, and information on this interesting phenomenon will be presented. An update on the use of TCBZ for human fascioliasis is also given. The review will indicate what progress has been made, but will also highlight areas that remain inadequately understood and require greater research focus.

Type
Review Article
Information
Journal of Helminthology , Volume 83 , Special Issue 2: Symposium and related papers from the 10th European Multicolloquium of Parasitology , June 2009 , pp. 139 - 150
Copyright
Copyright © Cambridge University Press 2009

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References

Akhtar, M.S., Iqbal, Z., Khan, M.N. & Lateef, M. (2000) Anthelmintic activity of medicinal plants with particular reference to their use in animals in the Indo-Pakistan subcontinent. Small Ruminant Research 38, 99–107.CrossRefGoogle Scholar
Albonico, M. (2003) Methods to sustain drug efficacy in helminth control programmes. Acta Tropica 86, 233–242.CrossRefGoogle ScholarPubMed
Alvarez, L.I., Solana, H.D., Mottier, M.L., Virkel, G.L., Fairweather, I. & Lanusse, C.E. (2005) Altered drug influx/efflux and enhanced metabolic activity in triclabendazole-resistant liver flukes. Parasitology 131, 501–510.CrossRefGoogle ScholarPubMed
Alvarez, A.I., Merino, G., Molina, A.J., Pulido, M.M., McKellar, Q.A. & Prieto, J.G. (2006) Role of ABC transporters in veterinary drug research and parasite resistance. Current Drug Delivery 3, 199–206.CrossRefGoogle ScholarPubMed
Alvarez-Sánchez, M.A., Mainar-Jaime, R.C., Pérez-García, J. & Rojo-Vázquez, F.A. (2006) Resistance of Fasciola hepatica to triclabendazole in sheep in Spain. Veterinary Record 159, 424–425.CrossRefGoogle ScholarPubMed
Alvinerie, M., Dupuy, J., Eeckhoutte, C. & Sutra, J.F. (1999) Enhanced absorption of pour-on ivermectin formulation in rats by co-administration of the multidrug-resistant-reversing agent verapamil. Parasitology Research 85, 920–922.CrossRefGoogle ScholarPubMed
Anthony, J.-P., Fyfe, L. & Smith, H. (2005) Plant active components – a resource for antiparasitic agents? Trends in Parasitology 21, 462–468.Google Scholar
Ballent, M., Lifschitz, A., Virkel, G., Sallovitz, J. & Lanusse, C. (2006) Modulation of the P-glycoprotein-mediated intestinal secretion of ivermectin: in vitro and in vivo assessments. Drug Metabolism and Disposition 34, 457–463.CrossRefGoogle ScholarPubMed
Ballent, M., Lifschitz, A., Virkel, G., Sallovitz, J. & Lanusse, C. (2007) Involvement of P-glycoprotein on ivermectin kinetic behaviour in sheep: itraconazole-mediated changes on gastrointestinal disposition. Journal of Veterinary Pharmacology and Therapeutics 30, 242–248.CrossRefGoogle ScholarPubMed
Barduagni, P., Hassanein, Y., Mohamed, M., El Wakeel, A., El Sayed, M., Hallaj, Z. & Curtale, F. (2008) Use of triclabendazole for treatment of patients co-infected by Fasciola spp. and S. mansoni in Behera Governate, Egypt. Parasitology Research 102, 631–633.CrossRefGoogle Scholar
Barnes, E.H., Dobson, R.J. & Barger, I.A. (1995) Worm control and anthelmintic resistance: adventures with a model. Parasitology Today 11, 56–63.CrossRefGoogle ScholarPubMed
Benchaoui, H. & McKellar, Q.A. (1996) Interaction between fenbendazole and piperonyl butoxide: pharmacokinetic and pharmacodynamic implications. Journal of Pharmacy and Pharmacology 48, 753–759.Google Scholar
Bennet, E.V., Behm, C., Bryant, C. & Chevis, R.A.F. (1980) Synergistic action of mebendazole and levamisole in the treatment of a benzimidazole-resistant Haemonchus contortus in sheep. Veterinary Parasitology 7, 207–214.Google Scholar
Borgsteede, F.H.M., Moll, L., Vellema, P. & Gaasenbeek, C.P.H. (2005) Lack of reversion in triclabendazole-resistant Fasciola hepatica. Veterinary Record 156, 350–351.CrossRefGoogle ScholarPubMed
Borstnik, K., Paik, I.-H., Shapiro, T.A. & Posner, G.H. (2002) Antimalarial chemotherapeutic peroxides: artemisinin, yinghaosu A and related compounds. International Journal for Parasitology 32, 1661–1667.CrossRefGoogle ScholarPubMed
Büscher, G., Bowen, F.L., Strong, M.B. & Crowfoot, P.D. (1999) Efficacy of triclabendazole, its metabolites and other compounds in sheep. 17th International Conference of the WAAVP, Copenhagen, 15–19 August, abstract c7.40.Google Scholar
Calvopiña, M., Guderian, R.H., Paredes, W. & Cooper, P.J. (2003) Comparison of two single-day regimens of triclabendazole for the treatment of human pulmonary paragonimiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 451–454.CrossRefGoogle ScholarPubMed
Coles, G.C. & Stafford, K.A. (2001) Activity of oxyclozanide, nitroxynil, clorsulon and albendazole against adult triclabendazole-resistant Fasciola hepatica. Veterinary Record 148, 723–724.Google Scholar
Coles, G.C., Rhodes, A.C. & Stafford, K.A. (2000) The activity of closantel against adult triclabendazole-resistant Fasciola hepatica. Veterinary Record 146, 504.CrossRefGoogle ScholarPubMed
Crump, A. (2006) New medicines from nature's armamentarium. Trends in Parasitology 22, 51–54.CrossRefGoogle ScholarPubMed
Curtale, F. (2006) Treatment of fascioliasis in human infections: a reply. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 187–188.CrossRefGoogle Scholar
Curtale, F. (2008) Treatment of human fascioliasis with triclabendazole: good news. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 508.CrossRefGoogle ScholarPubMed
Curtale, F., Hassanein, Y.A.E.W. & Savioli, L. (2005) Control of human fascioliasis by selective chemotherapy: design, cost and effect of the first public health, school-based intervention implemented in endemic areas of the Nile Delta, Egypt. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 599–609.CrossRefGoogle ScholarPubMed
Das, B., Tandon, V. & Saha, N. (2007) Genistein from Flemingia vestita (Fabaceae) enhances NO and its mediator (cGMP) production in a cestode parasite, Raillietina echinobothridia. Parasitology 134, 1457–1463.CrossRefGoogle Scholar
Das, B., Tandon, V., Lyndem, L.L., Gray, A.I. & Ferro, V.A. (2009) Phytochemicals from Flemingia vestita (Fabaceae) and Stephania glabra (Menispermeaceae) alter cGMP concentration in the cestode Raillietina echinobothrida. Comparative Biochemistry and Physiology part C, 149, 397–403.Google ScholarPubMed
Devine, C., Brennan, G.P., Lanusse, C.E., Alvarez, L.I., Trudgett, A., Hoey, E. & Fairweather, I. (2009) Effect of the metabolic inhibitor, methimazole on the drug susceptibility of a triclabendazole-resistant isolate of Fasciola hepatica. Parasitology 136, 183–192.CrossRefGoogle ScholarPubMed
Elard, L., Sauve, C. & Humbert, J.F. (1998) Fitness of benzimidazole-resistant and -susceptible worms of Teladorsagia circumcincta, a nematode parasite of small ruminants. Parasitology 117, 571–578.Google Scholar
El-Tantawy, W.H., Salem, H.F. & Mohammed Safwat, N.A.S. (2007) Effect of fascioliasis on the pharmacokinetic parameters of triclabendazole in human subjects. Pharmacy World and Science 29, 190–198.Google Scholar
Fairweather, I. (2005) Triclabendazole: new skills to unravel an old(ish) enigma. Journal of Helminthology 79, 227–234.CrossRefGoogle ScholarPubMed
Fairweather, I. & Boray, J.C. (1999) Fasciolicides: efficacy, actions, resistance and its management. Veterinary Journal 158, 81–112.CrossRefGoogle ScholarPubMed
Fairweather, I., Meaney, M., Savage, J., Brennan, G., Hoey, E. & Trudgett, A. (2008) The role of drug efflux pumps in the development of resistance to triclabendazole in Fasciola hepatica. Xth European Multicolloquium of Parasitology (EMOP X), Paris, August, abstract SY21/01–03.Google Scholar
Fetterer, R.H. (1986) The effect of albendazole and triclabendazole on colchicine binding in the liver fluke Fasciola hepatica. Journal of Veterinary Pharmacology and Therapeutics 9, 49–54.Google Scholar
Ghisi, M., Kaminsky, R. & Mäser, P. (2007) Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Veterinary Parasitology 144, 313–320.CrossRefGoogle ScholarPubMed
Halferty, L., Brennan, G.P., Hanna, R.E.B., Edgar, H.W., Meaney, M., McConville, M., Trudgett, A., Hoey, L. & Fairweather, I. (2008) Tegumental surface changes in juvenile Fasciola hepatica in response to treatment in vivo with triclabendazole. Veterinary Parasitology 155, 49–58.Google Scholar
Halferty, L., Brennan, G.P., Trudgett, A., Hoey, L. & Fairweather, I. (2009) Relative activity of triclabendazole metabolites against the liver fluke, Fasciola hepatica. Veterinary Parasitology 159, 126–138.CrossRefGoogle ScholarPubMed
Hammond, J.A., Fielding, D. & Bishop, S.C. (1997) Prospects for plant anthelmintics in tropical veterinary medicine. Veterinary Research Communications 21, 213–228.Google Scholar
Hanna, R.E.B., Edgar, H., Moffett, D., McConnell, S., Fairweather, I., Brennan, G.P., Trudgett, A., Hoey, E.M., Cromie, L., Taylor, S.M. & Daniel, R. (2008) Fasciola hepatica: histology of the testis in egg-producing adults of several laboratory-maintained isolates of flukes grown to maturity in cattle and sheep and in flukes from naturally infected hosts. Veterinary Parasitology 157, 222–234.CrossRefGoogle ScholarPubMed
Hegazi, A.G., Abd El Hady, F.K. & Shalaby, H.A. (2007a) An in vitro effect of propolis on adult worms of Fasciola gigantica. Veterinary Parasitology 144, 279–286.CrossRefGoogle Scholar
Hegazi, A.G., Abd El Hady, F.K. & Shalaby, H.A. (2007b) Inhibitory effect of Egyptian propolis on Fasciola hepatica eggs with reference to its effect on Clostridium oedematiens and correlation to chemical composition. Pakistan Journal of Biological Sciences 10, 3295–3305.Google Scholar
Hennessy, D.R., Lacey, E., Steel, J.W. & Prichard, R.K. (1987) The kinetics of triclabendazole disposition in sheep. Journal of Veterinary Pharmacology and Therapeutics 10, 64–72.CrossRefGoogle ScholarPubMed
Hien, T.T., Truong, N.T., Minh, N.H., Dat, H.D., Dung, N.T., Hue, N.T., Dung, T.K., Tuan, P.Q., Campbell, J.I., Farrar, J.J. & Day, J.N. (2008) A randomised controlled pilot study of artesunate versus triclabendazole for human fascioliasis in Central Vietnam. American Journal of Tropical Medicine and Hygiene 78, 388–392.Google Scholar
Higashi, K.O. & de Castro, S.L. (1994) Propolis extracts are effective against Trypanosoma cruzi and have an impact on its interaction with host cells. Journal of Ethnopharmacology 43, 149–155.CrossRefGoogle ScholarPubMed
Hopkins, T.J. & Gyr, P. (1991) Synergism of a combination of febantel and pyrantel emboate against Ancylostoma caninum on dogs. Veterinary Medical Review 61, 3–9.Google Scholar
Iqbal, Z., Akhtar, M.S., Sindhu, Z., Khan, M. & Jabbar, A. (2003) Herbal dewormers in livestock – a traditional therapy. International Journal of Agriculture and Biology 2, 199–206.Google Scholar
Kayser, O., Kiderlen, A.F. & Croft, S. (2003) Natural products as antiparasitic drugs. Parasitology Research 90, S55–S62.CrossRefGoogle ScholarPubMed
Keiser, J. & Morson, G. (2008a) Fasciola hepatica: tegumental alterations in adult flukes following in vitro and in vivo administration of artesunate and artemether. Experimental Parasitology 118, 228–237.CrossRefGoogle ScholarPubMed
Keiser, J. & Morson, G. (2008b) Fasciola hepatica: surface tegumental responses to in vitro and in vivo treatment with the experimental fasciolicide OZ78. Experimental Parasitology 119, 87–93.CrossRefGoogle ScholarPubMed
Keiser, J. & Utzinger, J. (2007a) Food-borne trematodiasis: current chemotherapy and advances with artemisinins and synthetic trioxolanes. Trends in Parasitology 23, 555–562.Google Scholar
Keiser, J. & Utzinger, J. (2007b) Artemisinins and synthetic trioxolanes in the treatment of helminth infections. Current Opinion in Infectious Diseases 20, 605–612.CrossRefGoogle ScholarPubMed
Keiser, J., Engels, D., Buscher, G. & Utzinger, J. (2005) Triclabendazole for the treatment of fascioliasis and paragonimiasis. Expert Opinion in Investigational Drugs 14, 1513–1526.CrossRefGoogle ScholarPubMed
Keiser, J., Xiao, S.-H., Jian, X., Chang, Z.-S., Odematt, P., Tesana, S., Tanner, M. & Utzinger, J. (2006a) Effect of artesunate and artemether against Clonorchis sinensis and Opisthorchis viverrini in rodent models. International Journal of Antimicrobial Agents 28, 370–373.CrossRefGoogle ScholarPubMed
Keiser, J., Brun, R., Fried, B. & Utzinger, J. (2006b) Trematocidal activity of praziquantel and artemisinin derivatives: in vitro and in vivo investigations on adult Echinostoma caproni. Antimicrobial Agents and Chemotherapy 50, 803–805.CrossRefGoogle ScholarPubMed
Keiser, J., Utzinger, J., Tanner, M., Dong, Y. & Vennerstrom, J.L. (2006c) The synthetic peroxide OZ78 is effective against Echinostoma caproni and Fasciola hepatica. Journal of Antimicrobial Chemotherapy 58, 1193–1197.CrossRefGoogle ScholarPubMed
Keiser, J., Shu-Hua, X., Tanner, M. & Utzinger, J. (2006d) Artesunate and artemether are effective fasciolicides in the rat model and in vitro. Journal of Antimicrobial Chemotherapy 57, 1139–1145.Google Scholar
Keiser, J., Utzinger, J., Vennerstrom, J.L., Dong, Y., Brennan, G.P. & Fairweather, I. (2007a) Activity of artemether and OZ78 against triclabendazole-resistant Fasciola hepatica. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 1219–1222.Google Scholar
Keiser, J., Shu-Hua, X., Chollet, J., Tanner, M. & Utzinger, J. (2007b) Evaluation of the in vivo activity of tribendimidine against Schistosoma mansoni, Fasciola hepatica, Clonorchis sinensis and Opisthorchis viverrini. Antimicrobial Agents and Chemotherapy 51, 1096–1098.CrossRefGoogle ScholarPubMed
Keiser, J., Xiao, S.H., Dong, Y., Utzinger, J. & Vennerstrom, J.L. (2007c) Clonorchicidal properties of the synthetic trioxolane OZ78. Journal of Parasitology 93, 1208–1213.CrossRefGoogle ScholarPubMed
Kelly, J.D., Whitlock, H.V., Thompson, H.V., Hall, C.A., Campbell, N.J., Martin, I.C.A. & Lejambre, L.F. (1978) Physiological characteristics of the free-living and parasitic stages of strains of Haemonchus contortus susceptible or resistant to benzimidazole anthelmintics. Research in Veterinary Science 25, 376–385.CrossRefGoogle ScholarPubMed
Kerboeuf, D., Blackhall, W., Kaminsky, R. & von Samson-Himmelstjerna, G. (2003) P-glycoprotein in helminths: function and perspectives for anthelmintic treatment and reversal of resistance. International Journal of Antimicrobial Agents 22, 332–346.CrossRefGoogle ScholarPubMed
Koko, W.S., Galal, M. & Khalid, H.S. (2000) Fasciolicidal efficacy of Albizia anthelmintica and Balanites aegyptiaca compared with albendazole. Journal of Ethnopharmacology 71, 247–252.Google Scholar
Lanusse, C.E. & Prichard, R.K. (1991) Enhancement of the plasma concentration of albendazole sulphoxide in sheep following coadministration of parenteral netobimin and liver oxidase inhibitors. Research in Veterinary Science 51, 306–312.CrossRefGoogle ScholarPubMed
Lanusse, C.E. & Prichard, R.K. (1992) Methimazole increases the plasma concentrations of the albendazole metabolites of netobimin in sheep. Biopharmaceutics and Drug Disposition 13, 95–103.Google Scholar
Lespine, A., Alvinerie, M., Vercruysse, J., Prichard, R. & Geldhof, P. (2008) ABC transporter modulation: a strategy to enhance the activity of macrocyclic lactone anthelmintics. Trends in Parasitology 24, 293–298.Google Scholar
Li, Y. & Wu, Y.-L. (2003) An over four millennium story behind qinghaosu (artemisinin) – a fantastic antimalarial drug from a traditional Chinese herb. Current Medicinal Chemistry 10, 2197–2230.Google Scholar
Lifschitz, A., Virkel, G., Ballent, M., Sallovitz, J. & Lanusse, C. (2009) Combined use of ivermectin and triclabendazole in sheep: in vitro and in vivo characterisation of their pharmacological interaction. Veterinary Journal, in press.Google Scholar
López-Garcia, M.L., Torrado, S., Torrado, S., Martinez, A.R. & Bolás, F. (1998) Methimazole-mediated enhancement of albendazole oral bioavailability and anthelmintic effects against parenteral stages of Trichinella spiralis in mice: the influence of the dose-regime. Veterinary Parasitology 75, 209–219.Google Scholar
Maingi, N., Scott, M.E. & Prichard, R.K. (1990) Effect of selection pressure for thiabendazole resistance on fitness of Haemonchus contortus in sheep. Parasitology 100, 327–335.CrossRefGoogle ScholarPubMed
Mas-Coma, S., Bargues, M.D. & Valero, M.A. (2005) Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 1255–1278.Google Scholar
McConville, M., Brennan, G.P., McCoy, M., Castillo, R., Hernández-Campos, A. & Fairweather, I. (2006) Adult triclabendazole-resistant Fasciola hepatica: surface and subsurface tegumental responses to in vitro treatment with the sulphoxide metabolite of the experimental fasciolicide compound alpha. Parasitology 133, 195–208.Google Scholar
McConville, M., Brennan, G.P., McCoy, M., Castillo, R., Hernández-Campos, A., Ibarra, F. & Fairweather, I. (2007) Immature triclabendazole-resistant Fasciola hepatica: tegumental responses to in vitro treatment with the sulphoxide metabolite of the experimental fasciolicide compound alpha. Parasitology Research 100, 365–377.Google Scholar
McConville, M., Brennan, G.P., Flanagan, A., Edgar, H.W.J., McCoy, M., Castillo, R., Hernández-Campos, A. & Fairweather, I. (2008) Surface and internal tegumental changes in juvenile Fasciola hepatica following treatment in vivo with the experimental fasciolicide, compound alpha. Veterinary Parasitology 153, 52–64.CrossRefGoogle ScholarPubMed
McConville, M., Brennan, G.P., Flanagan, A., Edgar, H.W.J., Hanna, R.E.B., McCoy, M., Gordon, A.W., Castillo, R., Hernández-Campos, A. & Fairweather, I. (2009a) An evaluation of the efficacy of compound alpha and triclabendazole against two isolates of Fasciola hepatica. Veterinary Parasitology, in press.Google Scholar
McConville, M., Brennan, G.P., Flanagan, A., Edgar, H.W.J., Castillo, R., Hernández-Campos, A. & Fairweather, I. (2009b) TEM ultrastructural changes to the tegumental system and the gastrodermal cells in mature flukes following in vivo treatment with the experimental fasciolicide, compound alpha. Parasitology, in press.Google Scholar
McCoy, M.A., Fairweather, I., Brennan, G.P., Kenny, J.M. & Forbes, A.B. (2005) The efficacy of nitroxynil and triclabendazole administered synchronously against juvenile triclabendazole-resistant Fasciola hepatica in sheep. Research in Veterinary Science 78, 33.Google Scholar
McKinstry, B., Brennan, G.P., Halferty, L., Forbes, A.B. & Fairweather, I. (2007) Ultrastructural changes induced in the tegument and gut of Fasciola hepatica following in vivo and in vitro drug treatment with nitroxynil (Trodax). Parasitology Research 101, 929–941.Google Scholar
McKinstry, B., Halferty, L., Brennan, G.P. & Fairweather, I. (2009) Morphological response of triclabendazole-resistant isolates of Fasciola hepatica to treatment in vitro with nitroxynil (Trodax). Parasitology Research 104, 645–655.Google Scholar
Meaney, M., Allister, J., McKinstry, B., McLaughlin, K., Brennan, G.P., Forbes, A.B. & Fairweather, I. (2006) Fasciola hepatica: morphological effects of a combination of triclabendazole and clorsulon against mature fluke. Parasitology Research 99, 609–621.Google Scholar
Meaney, M., Allister, J., McKinstry, B., McLauglin, K., Brennan, G.P., Forbes, A.B. & Fairweather, I. (2007) Fasciola hepatica: ultrastructural effects of a combination of triclabendazole and clorsulon against mature fluke. Parasitology Research 100, 1091–1104.Google Scholar
Merino, G., Molina, A.J., Garcia, J.L., Pulido, M.M., Prieto, J.G. & Alvarez, A.I. (2003) Intestinal elimination of albendazole sulfoxide: pharmacokinetic effects of inhibitors. International Journal of Pharmaceutics 263, 123–132.CrossRefGoogle ScholarPubMed
Mestorino, N., Formentini, E.A., Lucas, M.F., Fernandez, C., Modamio, P., Mariño Hernández, E. & Errecalde, J.O. (2008) Pharmacokinetic disposition of triclabendazole in cattle and sheep; discrimination of the order and the rate of the absorption process of its active metabolite triclabendazole sulfoxide. Veterinary Research Communications 32, 21–33.CrossRefGoogle ScholarPubMed
Molento, M.B. & Prichard, R.K. (1999) Effects of the multidrug-reversing agents verapamil and CL 347, 099 on the efficacy of ivermectin or moxidectin against unselected and drug-selected strains of Haemonchus contortus in jirds. Parasitology Research 85, 1007–1011.CrossRefGoogle ScholarPubMed
Moll, L., Gaasenbeek, C.P.H., Vellema, P. & Borgsteede, F.H.M. (2000) Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in the Netherlands. Veterinary Parasitology 91, 153–158.Google Scholar
Mottier, L., Virkel, G., Solana, H., Alvarez, L., Salles, J. & Lanusse, C. (2004) Triclabendazole biotransformation and comparative diffusion of the parent drug and its oxidised metabolites into Fasciola hepatica. Xenobiotica 34, 1043–1047.CrossRefGoogle Scholar
Mottier, L., Alvarez, L., Ceballos, L. & Lanusse, C. (2006a) Drug transport mechanisms in helminth parasites: passive diffusion of benzimidazole anthelmintics. Experimental Parasitology 113, 49–57.Google Scholar
Mottier, L., Alvarez, L., Fairweather, I. & Lanusse, C. (2006b) Resistance-induced changes in triclabendazole transport in Fasciola hepatica: ivermectin reversal effect. Journal of Parasitology 92, 1355–1360.Google Scholar
O'Neill, J.F., Johnston, R.C., Halferty, L., Brennan, G.P., Keiser, J. & Fairweather, I. (2009) Adult triclabendazole-resistant Fasciola hepatica: morphological responses to in vivo treatment with artemether in the rat model. Journal of Helminthology this issue.CrossRefGoogle Scholar
Ramírez, N., Mayet, L., Del Rivero, L., Ibarra-Velarde, F., Castillo, R., Hernández-Campos, A. & Jung-Cook, H. (2009) Pharmacokinetic behaviour in sheep and cattle of 5-chloro-2-(methylthio)-6-(1-naphthyloxy)-1H-benzimidazole, a new fasciolicide agent. Journal of Veterinary Pharmacology and Therapeutics, in press.Google Scholar
Rao, R.R. (1981) Ethnobotany of Meghalaya: medicinal plants used by Khasi and Garo tribes. Economic Botany 35, 4–9.Google Scholar
Reyes, P.M., Ibarra, V.F., Vera, M.Y., Cantó, A.G., Hernández, A., Hernández, C.A., Castillo, R. & Villa, M.A. (2008) Paramphistomicidal efficacy of an experimental compound in sheep. Parasitology Research 102, 705–708.Google Scholar
Rivero, L.M., Jung, H., Castillo, R. & Hernández-Campos, A. (1998) High-performance liquid chromatographic assay for a new fasciolicide agent, α-BIOF10, in biological fluids. Journal of Chromatography B 712, 237–241.CrossRefGoogle ScholarPubMed
Robinson, M.W., Trudgett, A., Hoey, E.M. & Fairweather, I. (2002) Triclabendazole-resistant Fasciola hepatica: β-tubulin and response to in vitro treatment with triclabendazole. Parasitology 124, 325–338.Google Scholar
Robinson, M.W., Lawson, J., Trudgett, A., Hoey, E.M. & Fairweather, I. (2004a) The comparative metabolism of triclabendazole sulphoxide by triclabendazole-susceptible and triclabendazole-resistant Fasciola hepatica. Parasitology Research 92, 205–210.CrossRefGoogle ScholarPubMed
Robinson, M.W., McFerran, N., Trudgett, A., Hoey, L. & Fairweather, I. (2004b) A possible model of benzimidazole binding to β-tubulin disclosed by invoking an inter-domain movement. Journal of Molecular Graphics and Modelling 23, 275–284.Google Scholar
Roy, B. & Tandon, V. (1999) Flukicidal activity of Alpinia nigra (Zingiberaceae) against the trematode, Fasciolopsis buski, in humans. Biomedical Letters 60, 23–29.Google Scholar
Ryan, L.A., Hoey, E., Trudgett, A., Fairweather, I., Fuchs, M., Robinson, M.W., Chambers, E., Timson, D., Ryan, E., Fetwell, T., Ivens, A., Bentley, G. & Johnston, D. (2008) Fasciola hepatica expresses multiple α- and β-tubulin isotypes. Molecular and Biochemical Parasitology 159, 73–78.Google Scholar
Sánchez, S., Small, J., Jones, D. & McKellar, Q.A. (2002) Plasma achiral and chiral pharmacokinetic behaviour of intravenous oxfendazole co-administered with piperonyl butoxide in sheep. Journal of Veterinary Pharmacology and Therapeutics 25, 7–13.Google Scholar
Sangster, N.C. (2001) Managing parasiticide resistance. Veterinary Parasitology 98, 89–109.Google Scholar
Shiramizu, K., Tuchida, T. & Anu, M. (1993) The anthelmintic effect on bovine fascioliasis of a crude preparation containing the root of Matteuccia orietalis. Journal of the Japan Veterinary Medical Association 46, 561–564.Google Scholar
Shoop, W.L., Ostlind, D.A., Rohrer, S.P., Mickle, G., Haines, H.W., Michael, B.F., Mrozik, H. & Fisher, M.H. (1995) Avermectins and Milbemycins against Fasciola hepatica: in vivo drug efficacy and in vitro receptor binding. International Journal for Parasitology 25, 923–927.Google Scholar
Shu-Hua, X., Jian, X., Tanner, M., Yong-Nian, Z., Keiser, J., Utzinger, J. & Hui-Qiang, Q. (2008) Artemether, artesunate, praziquantel and tribendimidine administered singly at different dosages against Clonorchis sinensis: a comparative in vivo study. Acta Tropica 106, 54–59.Google Scholar
Spicher, M., Roethlisberger, C., Lany, C., Stadelmann, B., Keiser, J., Ortega-Mora, L.M., Gottstein, B. & Hemphill, A. (2008) In vitro and in vivo treatments of Echinococcus protoscoleces and metacestodes with artemisinin and artemisinin derivatives. Antimicrobial Agents and Chemotherapy 52, 3447–3450.Google Scholar
Stepek, G., Lowe, A.E., Buttle, D.J., Duce, I.R. & Behnke, J.M. (2007) In vitro anthelmintic effects of cysteine proteinases from plants against intestinal helminths of rodents. Journal of Helminthology 81, 353–360.Google Scholar
Tagboto, S. & Townson, S. (2001) Antiparasitic properties of medicinal plants and other naturally occurring products. Advances in Parasitology 50, 198–295.Google ScholarPubMed
Toner, E., Brennan, G.P., Wells, K., McGeown, J.G. & Fairweather, I. (2008) Physiological and morphological effects of genistein against the liver fluke, Fasciola hepatica. Parasitology 135, 1189–1203.Google Scholar
Toner, E., McConvery, F., Brennan, G.P., Meaney, M. & Fairweather, I. (2009) A scanning electron microscope study on the route of entry of triclabendazole into the liver fluke, Fasciola hepatica. Parasitology, in press.CrossRefGoogle Scholar
Utzinger, J. & Keiser, J. (2004) Schistosomiasis and soil-transmitted helminthiasis: common drugs for treatment and control. Expert Opinion on Pharmacotherapy 5, 263–285.Google Scholar
Utzinger, J., Xiao, S.-H., Tanner, M. & Keiser, J. (2007) Artemisinins for schistosomiasis and beyond. Current Opinion in Investigational Drugs 8, 105–116.Google Scholar
Vennerstrom, J.L., Arbe-Barnes, S., Brun, R., Charman, S.A., Chiu, F.C.K., Chollet, J., Dong, Y., Dorn, A., Hunziker, D., Matile, H., McIntosh, K., Padmanilayam, M., Tomas, J.S., Scheurer, C., Scorneaux, B., Tang, Y., Urwyler, H., Wittlin, S. & Charman, W.N. (2004) Identification of an antimalarial synthetic trioxolane drug development candidate. Nature 430, 900–904.Google Scholar
Virkel, G., Lifschitz, A., Sallovitz, J., Pis, A. & Lanusse, C. (2006) Assessment of the main metabolism pathways for the flukicidal compound triclabendazole in sheep. Journal of Veterinary Pharmacology and Therapeutics 29, 213–223.Google Scholar
Virkel, G., Lifschitz, A., Sallovitz, J., Ballent, M., Scarcella, S. & Lanusse, C. (2009) Inhibition of cytochrome P450 activity enhances the systemic availability of triclabendazole metabolites in sheep. Journal of Veterinary Pharmacology and Therapeutics 32, 79–86.CrossRefGoogle ScholarPubMed
Walker, S.M., Hoey, E., Fletcher, H., Brennan, G., Fairweather, I. & Trudgett, A. (2006) Stage-specific differences in fecundity over the life-cycle of two characterized isolates of the liver fluke, Fasciola hepatica. Parasitology 133, 209–216.CrossRefGoogle ScholarPubMed
WHO (2007) Report of the WHO Informal Meeting on use of triclabendazole in fascioliasis control, held at WHO Headquarters, Geneva, Switzerland, October 2006. 39 pp. Geneva, WHO.Google Scholar
Wolstenholme, A.J., Fairweather, I., Prichard, R., von Samson-Himmelstjerna, G. & Sangster, N.C. (2004) Drug resistance in veterinary helminths. Trends in Parasitology 20, 469–476.CrossRefGoogle ScholarPubMed
Woodrow, C.J., Haynes, R.K. & Krishna, S. (2005) Artemisinins. Postgraduate Medical Journal 81, 71–78.Google Scholar
Xiao, S.-H. (2005) Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemisinins. Acta Tropica 96, 153–167.Google Scholar
Xiao, S.-H., Wu, Y.-L., Tanner, M., Wu, W.-M., Utzinger, J., Mei, J.-Y., Scorneaux, B., Chollet, J. & Zhai, Z. (2003) Schistosoma japonicum: in vitro effects of artemether combined with haemin depend on cultivation media and appraisal of artemether products appearing in the media. Parasitology Research 89, 459–466.CrossRefGoogle ScholarPubMed
Xue, J., Utzinger, J., Zhang, Y.-N., Tanner, M., Keiser, J. & Xiao, S.-H. (2008) Artemether and tribendimidine lack activity in experimemtal treatment of Paragonimus westermani in the dog. Parasitology Research 102, 537–540.CrossRefGoogle Scholar