Development of an egg hatch assay for the diagnosis of triclabendazole resistance in Fasciola hepatica: Proof of concept

Veterinary Parasitology

Volumn 183, Issue 3-4, 2012, Pages 249-259

  Fairweather, I ^a   McShane, D D ^a   Shaw, L ^a   Ellison, S E ^a   O'Hagan, N T ^a   York, E A ^a   Trudgett, A ^a   Brennan, G P ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

Egg hatch assay; Fasciola hepatica; Liver fluke; Liver fluke isolates; Triclabendazole; Triclabendazole resistance

Indexed keywords

TRICLABENDAZOLE;

ARTICLE; ASSAY; CELL DIVISION; CONCENTRATION RESPONSE; DEVELOPMENTAL STAGE; DRUG RESISTANCE; DRUG SENSITIVITY; EGG HATCH ASSAY; FASCIOLA HEPATICA; HATCHING; NONHUMAN; PARASITE ISOLATION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIPLATYHELMINTIC AGENTS; BENZIMIDAZOLES; CATTLE; CATTLE DISEASES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE; FASCIOLA HEPATICA; OVUM; PARASITIC SENSITIVITY TESTS; SHEEP; SHEEP DISEASES; SPECIES SPECIFICITY; SULFOXIDES;

FASCIOLA HEPATICA;

EID: 83255176873     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2011.07.023     Document Type: Article

References (70)

1. Albonico M., Wright V., Ramsan M., Haji H.J., Taylor M., Savioli L., Bickle Q. Development of the egg hatch assay for detection of anthelmintic resistance in human hookworms. Int. J. Parasitol. 2005, 35:803-811.
2. Alvarez L., Solana H., Mottier L., Virkel G., Fairweather I., Lanusse C.E. Altered drug influx/efflux and enhanced metabolic activity in triclabendazole-resistant liver flukes. Parasitology 2005, 131:501-510.
3. Alvarez L., Moreno G., Moreno L., Ceballos L., Shaw L., Fairweathet I., Lanusse C. Comparative assessment of albendazole and triclabendazole ovicidal activity on Fasciola hepatica eggs. Vet. Parasitol. 2009, 164:211-216.
4. Alvarez-Sánchez M.A., Mainar-Jaime R.C., Pérez-García J., Rojo-Vázquez F.A. Resistance of Fasciola hepatica to triclabendazole and albendazole in sheep in Spain. Vet. Rec. 2006, 159:424-425.
5. Boersema J.H., Lewing-van der Wiel P.J., Borgsteede F.H.M. Benzimidazole resistance in a field strain of Haemonchus contortus in the Netherlands. Vet. Rec. 1982, 110:203-204.
6. Boes J., Eriksen L., Nansen P. Embryonation and infectivity of Ascaris suum eggs isolated from worms expelled by pigs treated with albendazole, pyrantel pamoate, ivermectin or piperazine dihydrochloride. Vet. Parasitol. 1998, 75:181-190.
7. Borgsteede F.H.M., Moll L., Vellema P., Gaasenbeek C.P.H. Lack of reversion in triclabendazole-resistant Fasciola hepatica. Vet. Rec. 2005, 156:350-351.
8. Büscher G., Bowen F.L., Strong M.B., Allison J.R., Richards R.J. Extension of the prepatent period of Fasciola hepatica in infected animals following treatment with triclabendazole. Vet. Rec. 1987, 120:460-461.
9. Chowaniec W., Darski J. Investigations on excretion time of liver fluke eggs after killing the parasite. Bull. Vet. Inst. Pulway 1970, 14:108-110.
10. Coles G.C. Anthelmintic resistance - looking to the future: a UK perspective. Res. Vet. Sci. 2005, 78:99-108.
11. Coles G.C., Briscoe M.G. Benzimidazoles and fluke eggs. Vet. Rec. 1978, 103:360-361.
12. Coles G.C., Simpkin K.G. Resistance of nematode eggs to the ovicidal activity of benzimidazoles. Res. Vet. Sci. 1977, 22:386-387.
13. Coles G.C., Bauer C., Borgsteede F.H.M., Geerts S., Klei T.R., Taylor M.A., Waller P.J. World Association for the Advancement of Veterinaryt Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 1992, 44:35-44.
14. Coles G.C., Jackson F., Pomroy W.E., Prichard R.K., von Samson-Himmelstjerna G., Silvestre A., Taylor M.A., Vercruysse J. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 2006, 136:167-185.
15. DEFRA, 2003. Final report for project (OD0540), entitled " Development of systems for monitoring anthelmintic resistance in the field" DEFRA, London.
16. Devine C., Brennan G.P., Lanusse C.E., Alvarez L.I., Trudgett A., Hoey E., Fairweather I. Effect of the metabolic inhibitor, methimazole on the drug susceptibility of a triclabendazole-resistant isolate of Fasciola hepatica. Parasitology 2009, 136:183-192.
17. Devine C., Brennan G.P., Lanusse C.E., Alvarez L.I., Trudgett A., Hoey E.M., Fairweather I. Inhibition of cytochrome P450-mediated metabolism enhances ex vivo susceptibility of Fasciola hepatica to triclabendazole. Parasitology 2010, 137:871-880.
18. Devine C., Brennan G.P., Lanusse C.E., Alvarez L.I., Trudgett A., Hoey E., Fairweather I. Potentiation of triclabendazole sulphoxide-induced tegumental disruption by methimazole in a triclabendazole-resistant isolate of Fasciola hepatica. Parasitol. Res. 2010, 106:1351-1363.
19. Devine C., Brennan G.P., Lanusse C.E., Alvarez L.I., Trudgett A., Hoey E., Fairweather I. Enhancement of the drug susceptibility of a triclabendazole-resistant isolate of Fasciola hepatica using the metabolic inhibitor ketoconazole. Parasitol. Res. 2010, 107:337-353.
20. Devine C., Brennan G.P., Lanusse C.E., Alvarez L.I., Trudgett A., Hoey E., Fairweather I. Piperonyl butoxide enhances triclabendazole action against triclabendazole-resistant Fasciola hepatica. Parasitology 2011, 138:224-236.
21. Devine C., Brennan G.P., Lanusse C.E., Alvarez L.I., Trudgett A., Hoey E., Fairweather I. Enhancement of triclabendazole action in vivo against a triclabendazole-resistant isolate of Fasciola hepatica by co-treatment with ketoconazole. Vet. Parasitol. 2011, 177:305-315.
22. Devine, C., Brennan, G.P., Lanusse, C.E., Alvarez, L.I., Trudgett, A., Hoey, E., Fairweather, I. Inhibition of triclabendazole metabolism in vitro by ketoconazole increases disruption to the tegument of a triclabendazole-resistant isolate of Fasciola hepatica. Parasitol. Res., in press. doi:10.1007/s00436-011-2304-9.
23. Egerton J.R. The ovicidal and larvicidal effect of thiabendazole on various helminth species. Texas Rep. Biol. Med. 1969, 27:561-580.
24. Ennos A.R. Statistical and Data Handling Skills in Biology 2007, Prentice Hall, Harlow, Essex, UK. 2nd edition.
25. Fairweather I. Triclabendazole: new skills to unravel an old(ish) enigma. J. Helminthol. 2005, 79:227-234.
26. Fairweather I. Triclabendazole progress report, 2005-2009: an advancement of learning?. J. Helminthol. 2009, 83:139-150.
27. Fairweather I. Liver fluke isolates: a question of provenance. Vet. Parasitol. 2011, 176:1-8.
28. Fairweather I. Raising the bar on reporting cases of " triclabendazole resistance" Vet. Rec. 2011, 168:514-515.
29. Fairweather I. Reducing the future threat from (liver) fluke: realistic prospect or quixotic fantasy?. Vet. Parasitol. 2011, 180:133-143.
30. Flanagan A.M.E., Forster H.W.J., Gordon F., Hanna A., McCoy R.E.B., Brennan M., Fairweather G.P. Standardisation of a coproantigen reduction test (CRT) protocol for the diagnosis of resistance to triclabendazole in Fasciola hepatica. Vet. Parasitol. 2011, 176:34-42.
31. Flanagan A., Edgar H.W.J., Gordon A., Hanna R.E.B., Brennan G.P., Fairweather I. Comparison of two assays, a faecal egg count reduction test (FECRT) and a coproantigen reduction test (CRT), for the diagnosis of resistance to triclabendazole in Fasciola hepatica in sheep. Vet. Parasitol. 2011, 176:170-176.
32. Fox N.J., White P.C.L., McClean C.J., Marion G., Evans A., Hutchings M.R. Predicting impacts of climate change on Fasciola hepatica risk. PLoS One 2011, 6:e16126.
33. Hall C.A., Campbell N.J., Richardson N.J. Levels of benzimidazole resistance in Haemonchus contortus and Trichostrongylus colubriformis recorded from an egg hatch test procedure. Res. Vet. Sci. 1978, 25:360-363.
34. Hanna R.E.B., Cromie L., Taylor S.M., Couper A. The effect of a parenteral ivermectin/closantel injection on the growth and reproductive development of early immature Fasciola hepatica in cattle. Vet. Parasitol. 2006, 142:78-90.
35. Hanna R.E.B., Edgar H.W.J., McConnell S., Toner E., McConville M., Brennan G.P., Devine C., Flanagan A., Halferty L., Meaney M., Shaw L., Moffett D., McCoy M., Fairweather I. Fasciola hepatica: histological changes in the reproductive structures of triclabendazole (TCBZ)-sensitive and TCBZ-resistant flukes after treatment in vivo with TCBZ and the related benzimidazole derivative, Compound Alpha. Vet. Parasitol. 2010, 168:240-254.
36. Kenyon F., Sargison N.D., Skuce P.J., Jackson F. Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change. Vet. Parasitol. 2009, 163:293-297.
37. Kirsch R., Schleich H. Morphological changes in trichostrongylid eggs after treatment with fenbendazole. Vet. Parasitol. 1982, 11:375-380.
38. Lacey E. The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug-resistance to benzimidazoles. Int. J. Parasitol. 1998, 18:885-936.
39. Lang B.Z., Hall R.F., Kirstein K.W., Wescott R.B. Reduced reproductive potential of Fasciola hepatica surviving in cattle treated with albendazole. Vet. Med. Small Anim. Clin. 1980, 75:1853-1857.
40. Le Jambre L.F. Egg hatch as an in vitro assay of thiabendazole resistance in nematodes. Vet. Parasitol. 1976, 2:385-391.
41. Lucas J.M.S. 4-Cyano-2-iodo-6-nitrophenol, M&B 10,775. I: activity against experimental fascioliasis in rabbits, sheep and calves. Br. Vet. J 1967, 123:198-211.
42. Maes L., Lauwers H., Deckers W., Vanparijs O. Flukicidal action of closantel against immature and mature Fasciola hepatica in experimentally infected rats and sheep. Res. Vet. Sci. 1988, 44:229-232.
43. Maes L., Vanparijs O., Lauwers H., Deckers W. Comparative efficacy of closantel and triclabendazole against Fasciola hepatica in experimentally infected sheep. Vet. Rec. 1990, 127:450-452.
44. Maisonneuve H., Rossignol J.F., Addo A., Mojon M. Ovicidal effects of albendazole in human ascariasis, ancylostomiasis and trichuriasis. Ann. Trop. Med. Parasitol. 1985, 79:79-82.
45. Malone J.B., Smith P.H., Loyacano A.F., Hembry F.G., Brock L.T. Efficacy of albendazole for treatment of naturally acquired Fasciola hepatica in calves. Am. J. Vet. Res. 1982, 43:879-881.
46. Malone J.B., Ramsey R.T., Loyacano A.F. Efficacy of clorsulon for treatment of mature naturally acquired and 8-week-old experimentally induced Fasciola hepatica infections in cattle. Am. J. Vet. Res. 1984, 45:851-854.
47. McCann C.M., Baylis M., Williams D.J.L. The development of linear regression models using environmental variables to explain the spatial distribution of Fasciola hepatica infection in dairy herds in England and Wales. Int. J. Parasitol. 2010, 40:1021-1028.
48. McConville M., Brennan G.P., McCoy M., Castillo R., Hernández-Campos A., Ibarra F., Fairweather I. 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 2006, 133:195-208.
49. 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. An evaluation of the efficacy of compound alpha and triclabendazole against two isolates of Fasciola hepatica. Vet. Parasitol. 2009, 162:75-88.
50. McConville M., Hanna R.E.B., Brennan G.P., McCoy M., Edgar H.W.J., McConnell S., Castillo R., Hernández-Campos A., Fairweather I. Fasciola hepatica: disruption of spermatogenesis by the fasciolicide compound alpha. Parasitol. Res. 2010, 106:311-323.
51. Mezo M., González-Warleta M., Ubeira F.M. The use of MM3 monoclonal antibodies for the early immunodiagnosis of ovine fascioliasis. J. Parasitol. 2007, 93:65-72.
52. Miller J.E., Morrison D.G. Effect of fenbendazole and ivermectin on development of strongylate nematode eggs and larvae in calf feces. Vet. Prasitol. 1992, 43:265-270.
53. Mottier L., Virkel G., Solana H., Alvarez L., Salles J., Lanusse C. Triclabendazole biotransformation and comparative diffusion of the parent drug and its oxidised metabolites into Fasciola hepatica. Xenobiotica 2004, 34:1043-1057.
54. Mottier L., Alvarez L., Fairweather I., Lanusse C. Resistance-induced changes in triclabendazole transport in Fasciola hepatica: ivermectin reversal effect. J. Parasitol. 2006, 92:1355-1360.
55. Rinaldi G., Morales M.E., Alrefaei Y.N., Cancela M., Castillo E., Dalton J.P., Tort J.F., Brindley P.J. RNA interference targeting leucine aminopeptidase blocks hatching of Schistosoma mansoni eggs. Mol. Biochem. Parasitol. 2009, 167:118-126.
56. Riou M., Koch C., Kerboeuf D. Increased resistance to anthelmintics of Haemonchus contortus eggs associated with changes in membrane fluidity of eggshells during embryonation. Parasitol. Res. 2005, 95:266-272.
57. Rokni M.B., Massoud J., O'Neill S.M., Parkinson M., Dalton J.P. Diagnosis of human fasciolosis in the Gilan province of Northern Iran: application of cathepsin L-ELISA. Diagn. Microbiol. Infect. Dis. 2002, 44:175-179.
58. Roush R.T., Miller G.L. Considerations for design of insecticide resistance monitoring programs. J. Econ. Entomol. 1986, 79:293-298.
59. Samizadeh-Yazd A., Todd A.C. Anthelmintic activities of fenbedazole against Nematodirus helvetianus in cattle: effect on egg production, embryogeny, and development of larval stages. Am. J. Vet. Res. 1978, 39:1668-1671.
60. Scarcella S., Fiel C., Guzman M., Alzola R., Felipe A., Hanna R.E.B., Fairweather I., McConnell S., Solana H. Reproductive disruption in Fasciola hepatica associated with incomplete efficacy of a new experimental formulation of triclabendazole. Vet. Parasitol. 2011, 176:157-164.
61. Taylor M.A., Hunt K.R., Goodyear K.L. Anthelmintic resistance detection methods. Vet. Parasitol. 2002, 103:183-194.
62. Thomas C., Jacquiet P., Dorchies P. La prévalence des helminthoses bovines a-t-elle été modifiée par la canicule de l'été 2003 dans le Sud-Ouest de la France?. Parasite 2007, 14:265-268.
63. Toner E., Brennan G.P., Hanna R.E.B., Edgar H.W.J., Fairweather I. Disruption of egg formation by Fasciola hepatica following treatment in vivo with triclabendazole in the sheep host. Vet. Parasitol. 2011, 177:79-89.
64. Toner, E., Brennan, G.P., Hanna, R.E.B., Edgar, H.W.J., Fairweather, I. Fasciola hepatica: time-dependent disruption of spermatogenesis following in vivo treatment with triclabendazole. Parasitol. Res., in press. doi:10.1007/s00436-011-2341-4.
65. van Dijk J., Sargison N.D., Kenyon F., Skuce P.J. Climate change and infectious disease: helminthological challenges to farmed ruminants in temperate regions. Animal 2010, 4:377-392.
66. Várady M., čudeková P., čorba J. In vitro detection of benzimidazole resistance in Haemonchus contortus: egg hatch test versus larval development test. Vet. Parasitol. 2007, 149:104-110.
67. von Samson-Himmelstjerna G., Coles G.C., Jackson F., Bauer C., Borgsteede F., Cirak V.Y., Demeler J., Donnan A., Dorny P., Epe C., Harder A., Höglund J., Kaminsky R., Kerboeuf D., Küttler U., Papadopoulos E., Posedi J., Small J., Várady M., Vercruysse J., Wirtherle N. Standardisation of the egg hatch test for the detection of benzimidazole resistance in parasitic nematodes. Parasitol. Res. 2009, 105:825-834.
68. Wagner E.D., Chavarria A.P. In vivo effects of a new anthelmintic, mebendazole (R-17,635) on the eggs of Trichuris trichiura and hookworm. Am. J. Trop. Med. Hyg. 1974, 23:151-153.
69. Walker S.M., Hoey E., Fletcher H., Brennan G.P., Fairweather I., Trudgett A. Stage-specific differences in fecundity over the life-cycle of two characterized isolates of the liver fluke Fasciola hepatica. Parasitology 2006, 133:209-216.
70. Xu Y.Z., Dresden M.H. Leucine aminopeptidase and hatching of Schistosoma mansoni eggs. J. Parasitol. 1986, 72:507-511.