Interference with P-glycoprotein improves ivermectin activity against adult resistant nematodes in sheep

Veterinary Parasitology

Volumn 172, Issue 3-4, 2010, Pages 291-298

  Lifschitz, A ^a,b   Entrocasso, C ^c   Alvarez, L ^a,b   Lloberas, M ^c   Ballent, M ^a,b   Manazza, G ^c   Virkel, G ^a,b   Borda, B ^c   Lanusse, C ^a,b  

^a UNIVERSIDAD NACIONAL DEL CENTRO DE LA PROVINCIA DE BUENOS AIRES   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

Author keywords

Ivermectin; Loperamide; P glycoprotein; Pharmacokinetics; Resistant nematodes; Sheep

Indexed keywords

GLYCOPROTEIN P; IVERMECTIN; LOPERAMIDE; LOPEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTHELMINTIC ACTIVITY; ARTICLE; BLOOD SAMPLING; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG DISPOSITION; DRUG EFFICACY; DRUG HALF LIFE; DRUG POTENTIATION; FECES ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MAXIMUM PLASMA CONCENTRATION; MONOTHERAPY; NEMATODIASIS; NONHUMAN; PLASMA CONCENTRATION-TIME CURVE; SHEEP DISEASE;

ANIMALS; ANTIDIARRHEALS; ANTIPARASITIC AGENTS; DRUG RESISTANCE; FECES; IVERMECTIN; LOPERAMIDE; NEMATODA; NEMATODE INFECTIONS; P-GLYCOPROTEIN; PARASITE EGG COUNT; SHEEP; SHEEP DISEASES;

ANIMALIA; HAEMONCHUS CONTORTUS; NEMATODA; OVIS ARIES; TRICHOSTRONGYLUS COLUBRIFORMIS;

EID: 77956012325     PISSN: 03044017     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetpar.2010.04.039     Document Type: Article

References (43)

1. Alvarez L., Mottier L., Lanusse C. Drug transfer into target helminth parasites. Trends Parasitol. 2007, 23:97-104.
2. Alvinerie M., Sutra J.F., Galtier P. Ivermectin in goat milk after subcutaneous injection. Vet. Res. 1993, 24:417-421.
3. Alvinerie M., Dupuy J., Kili-Mvouaka S., Sutra J., Lespine A. Ketoconazole increases the plasma levels of ivermectin in sheep. Vet. Parasitol. 2008, 157:117-122.
4. Anziani O.S., Suarez V., Guglielmone A.A., Warnke O., Grande H., Coles G.C. Resistance to benzimidazole and macrocyclic lactone anthelmintics in cattle nematodes in Argentina. Vet. Parasitol. 2004, 122:303-306.
5. Ballent M., Lifschitz A., Virkel G., Sallovitz J., Lanusse C. Modulation of the p-glycoprotein-mediated intestinal secretion of ivermectin: in vitro and in vivo assessments. Drug Metab. Dispos. 2006, 34:457-463.
6. Ballent M., Lifschitz A., Virkel G., Sallovitz J., Lanusse C. Involvement of P-glycoprotein on ivermectin kinetic behaviour in sheep: itraconazole-mediated changes on gastrointestinal disposition. J. Vet. Pharmacol. Ther. 2007, 30:242-248.
7. Barber S., Bowles V., Lespine A., Alvinerie M. The comparative serum disposition kinetics of subcutaneous administration of doramectin, ivermectin and moxidectin in the Australian merino sheep. J. Vet. Pharmacol. Ther. 2003, 26:343-348.
8. Bartley D.J., McAllister H., Bartley Y., Dupuy J., Ménez C., Alvinerie M., Jackson F., Lespine A. P-glycoprotein interfering agents potentiate ivermectin susceptibility in ivermectin sensitive and resistant isolates of Teladorsagia circumcincta and Haemonchus contortus. Parasitology 2009, 136:1081-1088.
9. Bartley D.J., Dupuy J., Alvinerie M., Jackson F., Lespine A. The influence of ketoconazole and Pluronic85 on the efficacy and pharmacokinetics of ivermectin in lambs infected with anthelmintic resistant Haemonchus contortus. Proceedings of 22nd International Conference of the World Association for the Advancement of Veterinary Parasitology, CS2.2, vol. 9 2009.
10. Blackhall W.J., Pouliot J.F., Prichard R.K., Beech R.N. Haemonchus contortus: selection at a glutamate-gated chloride channel gene in ivermectin- and moxidectin-selected strains. Exp. Parasitol. 1998, 90:42-48.
11. Coles G.C., Bauer F.H.M., Borgsteede S., Geerst T.R., Klei T.R., Taylor M.A., Waller P.J. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.). Methods for detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 1992, 44:35-44.
12. Crump A., Otoguro K. Satoshi Omura: in pursuit of nature's bounty. Trends Parasitol. 2005, 21:126-132.
13. Demeler J., Van Zeveren A.M., Kleinschmidt N., Vercruysse J., Höglund J., Koopmann R., Cabaret J., Claerebout E., Areskog M., von Samson-Himmelstjerna G. Monitoring the efficacy of ivermectin and albendazole against gastro intestinal nematodes of cattle in Northern Europe. Vet Parasitol. 2009, 160:109-115.
14. Demeler J., Krücken J., Al Gusbi S., von Samson-Himmelstjerna G. Cloning and functional characterization of a Cooperia oncophora P-glycoprotein A. Proceedings of 22nd International Conference of the World Association for the Advancement of Veterinary Parasitology, P02.10, pp 151 2009.
15. De Montigny P., Shim J.S., Pivnichny J.V. Liquid chromatographic determination of ivermectin in animal plasma with trifluoroacetic anhydride and N-methylimidazole as the derivatization reagent. J. Pharm. Biomed. Anal. 1990, 8:507-511.
16. Dicker A., Gilleard J., Skuce P., Nisbet A., Bartley D., Britton C., Jackson F. Ivermectin resistance - a role for gene expression?. Proceedings of 22nd International Conference of the World Association for the Advancement of Veterinary Parasitology, P01.18, pp 123 2009.
17. Dupuy J., Larrieu G., Sutra J.F., Lespine A., Alvinerie M. Enhancement of moxidectin bioavailability in lamb by a natural flavonoid: quercetin. Vet. Parasitol. 2003, 112:337-347.
18. El-Banna H.A., Goudah A., El-Zorba H., Abd-El-Rahman S. Comparative pharmacokinetics of ivermectin alone and a novel formulation of ivermectin and rafoxanide in calves and sheep. Parasitol. Res. 2008, 102:1337-1342.
19. Entrocasso C., Alvarez L., Manazza J., Lifschitz A., Borda B., Virkel G., Mottier L., Lanusse C. Clinical efficacy assessment of the albendazole-ivermectin combination in lambs parasitized with resistant nematodes. Vet. Parasitol. 2008, 155:249-256.
20. Geary T.G. Ivermectin 20 years on: maturation of a wonder drug. Trends Parasitol. 2005, 21:530-532.
21. Gibaldi M., Perrier D. Pharmacokinetics 1982, Marcel Dekker, Inc., New York, USA. 2nd edition Revised and Expanded.
22. Imperiale F., Lifschitz A., Sallovitz J., Virkel G., Lanusse C. Comparative depletion of ivermectin and moxidectin milk residues in dairy sheep after oral and subcutaneous administration. J. Dairy Res. 2004, 71:427-433.
23. Kaplan R.M. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol. 2004, 20:477-481.
24. Kerboeuf D., Guegnard F., Le Vern Y. Analysis and partial reversal of multidrug resistance to anthelmintics due to P-glycoprotein in Haemonchus contortus eggs using Lens culinaris lectin. Parasitol. Res. 2002, 88:816-821.
25. Kwa M.S.G., Okoli M.N., Schulz-Key H., Okongkwo P.O., Ross M.H. Use of P-glycoprotein gene probes to investigate antihelmintic resistance in Haemonchus contortus and comparison with Onchocerca volvulus. Int. J. Parasitol. 1998, 28:1235-1240.
26. Laffont C.M., Toutain P.L., Alvinerie M., Bousquet-Melou A. Intestinal secretion is a major route for parent ivermectin elimination in the rat. Drug Metab. Dispos. 2002, 30:626-630.
27. Lespine A., Martin S., Dupuy J., Roulet A., Pineau T., Orlowski S., Alvinerie M. Interaction of macrocyclic lactones with P-glycoprotein: structure-affinity relationship. Eur. J. Pharmacol. Sci. 2007, 30:84-94.
28. Lifschitz A., Virkel G., Pis A., Imperiale F., Sánchez S., Alvarez L., Kujanek R., Lanusse C. Ivermectin disposition kinetics after subcutaneous and intramuscular administration of an oil-based formulation to cattle. Vet. Parasitol. 1999, 86:203-215.
29. Lifschitz A., Virkel G., Sallovitz J., Imperiale F., Pis A., Lanusse C. Loperamide-induced enhancement of moxidectin availability in cattle. J. Vet. Pharmacol. Ther. 2002, 25:111-120.
30. Lifschitz A., Virkel G., Sallovitz J., Imperiale F., Pis A., Lanusse C. Loperamide modifies the tissue disposition kinetics of ivermectin in rats. J. Pharm. Pharmacol. 2004, 56:61-67.
31. Lifschitz A., Sallovitz J., Imperiale F., Suarez V., Cristel S., Ahoussou S., Lanusse C. Modulation of P-glycoprotein enhances ivermectin and moxidectin systemic availabilities and their efficacy against resistant nematodes in cattle. Exp. Parasitol. 2010, 10.1016/j.exppara.2010.01.009.
32. Lin J.H. Drug-drug interaction mediated by inhibition and induction of P-glycoprotein. Adv. Drug Deliv. Rev. 2003, 55:53-81.
33. Ling V., Thompson L.H. Reduced permeability in CHO cells as a mechanism of resistance to colchicine. J. Cell Physiol. 1974, 83:103-116.
34. Molento M.B., Prichard R.K. The effects of the multidrug-resistance-reversing agent verapamil and CL347,099 on the efficacy of ivermectin or moxidectin against unselected and drug-selected strains of Haemonchus contortus in jirds (Meriones unguiculatus). Parasitol. Res. 1999, 85:1007-1011.
35. Molento M., Lifschitz A., Sallovitz J., Lanusse C., Prichard R. Influence of verapamil on the pharmacokinetics of the antiparasitic drugs ivermectin and moxidectin in sheep. Parasitol. Res. 2004, 92:121-127.
36. Prichard R.K., Roulet A. ABC transporters and β-tubulin in macrocyclic lactones resistance: prospects for marker development. Parasitology 2007, 134:1123-1132.
37. Roberts F., O'Sullivan P. Methods for egg counts and larval cultures for strongyles infecting the gastrointestinal tract of cattle. Aust. J. Agric. Res. 1949, 1:99-103.
38. Sangster N.C., Bannan S.C., Weiss A.S., Nulf S.C., Klein R.D., Geary T.G. Haemonchus contortus: sequence heterogeneity of internucleotide binding domains from P-glycoproteins. Exp. Parasitol. 1999, 91:250-257.
39. Schinkel A., Smit J., van Telligen O., Beijnen J., Wagenaar E., van Deemter L., Mol C., van der Valk M., Rocabus-Maandag E., Riele H., Berns A., Borst P. Disruption of the mouse mdr1a P-Glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 1994, 77:491-502.
40. Schinkel A., Wagenaar E., Mol C., van Deemter L. P-glycoprotein in the blood-brain barrier of mice influences the brain penetration and pharmacological activity of many drugs. J. Clin. Invest. 1996, 97:2517-2524.
41. Xu M., Molento M., Blackhall W., Ribeiro P., Beech R., Prichard R. Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Mol. Biochem. Parasitol. 1998, 91:327-335.
42. Wood I.B., Amaral N.K., Bairden K., Duncan J.L., Kassai T., Malone J.B., Pankavich J.A., Reinecke R.K., Slocombe O., Taylor S.M., Vercruysse J. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) second edition of guidelines for evaluating the efficacy of anthelmintics in ruminants (bovine, ovine, caprine). Vet. Parasitol. 1995, 58:181-213.
43. Wolstenholme A., Fairweather I., Prichard R., von Samson-Himmelstjerna G., Sangster V. Drug resistance in veterinary parasites. Trends Parasitol. 2004, 20:469-476.