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Substitution of benzimidazole-resistant nematodes for susceptible nematodes in grazing lambs

Published online by Cambridge University Press:  13 November 2006

M.-N. MOUSSAVOU-BOUSSOUGOU ,
A. SILVESTRE ,
J. CORTET ,
C. SAUVE  and
J. CABARET
M.-N. MOUSSAVOU-BOUSSOUGOU
Affiliation:
INRA, UR1282 Animal Infectious Diseases and Public Health, F-37380 Nouzilly, France
A. SILVESTRE
Affiliation:
INRA, UR1282 Animal Infectious Diseases and Public Health, F-37380 Nouzilly, France
J. CORTET
Affiliation:
INRA, UR1282 Animal Infectious Diseases and Public Health, F-37380 Nouzilly, France
C. SAUVE
Affiliation:
INRA, UR1282 Animal Infectious Diseases and Public Health, F-37380 Nouzilly, France
J. CABARET
Affiliation:
INRA, UR1282 Animal Infectious Diseases and Public Health, F-37380 Nouzilly, France
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Abstract

Multi-drug-resistant gastrointestinal nematode parasite populations are becoming more and more prevalent. Since anthelmintic treatments are of limited effectiveness, one solution could be to replace the anthelmintic-resistant population by a susceptible population, in order to re-establish the possibility of drug-based anthelmintic control. We investigated this substitution strategy in 4 paddocks of 0·7 ha, each of which was seeded with a benzimidazole-resistant Teladorsagia circumcincta population. The proportion of benzimidazole-resistant worms in these paddocks ranged from 20% to 89%. A 2-step replacement was performed: first, the paddocks were not grazed for 6 months (from December to July), and then the grass was cut to eliminate any residual infective larvae, before contaminating each of the paddocks with 10 seeder lambs experimentally infected with a benzimidazole-susceptible strain of T. circumcincta (from July to November). At the end of the experiment, all the populations on the 4 paddocks were phenotypically benzimidazole-susceptible, but genotyping indicated that 2 populations harboured 1% and 3% resistant worms respectively. This study demonstrates that nematode replacement is feasible in temperate areas, using semi-intensive stock management, even when the initial levels of benzimidazole-resistance are very high. Further research should next assess replacing the whole community to cope with the species diversity observed under field conditions.

Keywords

nematode controlanthelmintic resistancereplacementsynthetic strainbenzimidazoleTeladorsagia circumcincta
Type
Research Article
Information
Parasitology , Volume 134 , Issue 4 , April 2007 , pp. 553 - 560
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Anonymous ( 2005). Les systèmes ovins lait en France: diversité des systèmes d'exploitation, repères techniques et économiques (Institut de l'élevage).
Aumont, G., Chevalier, M., Hostache, G., Mandonnet, N., Arquet, R., Cabaret, J. and Silvestre, A. ( 2002). Replacement of a helmintic community in Creole meat goats of Guadeloupe: a strategy to preserve genetic diversity of parasitic populations and to control anthelmintic resistance. In IVe National Colloquium of Bureau des Ressources Génétiques (BRG), La Châtre, France, 14–16 October 2002, pp. 37–38.Google Scholar
Aumont, G. and Gruner, L. ( 1989). Population evolution of the free-living stage of goat gastrointestinal nematodes on herbage under tropical conditions in Guadeloupe (French West Indies). International Journal for Parasitology 19, 539–546. DOI: 10.1016/0020-7519(89)90084-2CrossRefGoogle Scholar
Beaumont-Schwartz, C., Kerboeuf, D. and Hubert, J. ( 1987). Methods of detecting gastrointestinal strongyles resistant to anthelmintics. Recueil de Médecine Vétérinaire 163, 683–688.Google Scholar
Benchaoui, H. A. and McKellar, Q. A. ( 1996). Interaction between fenbendazole and piperonyl butoxide: Pharmacokinetic and pharmacodynamic implications. Journal of Pharmacy and Pharmacology 48, 753–759.CrossRefGoogle Scholar
Bird, J., Shulaw, W. P., Pope, W. F. and Bremer, C. A. ( 2001). Control of anthelmintic resistant endoparasites in a commercial sheep flock through parasite community replacement. Veterinary Parasitology 97, 219–225. DOI: 10.1016/S0304-4017(01)00406-XCrossRefGoogle Scholar
Borgsteede, F. H. M. and Duyn, S. P. J. ( 1989). Lack of reversion of a benzimidazole resistant strain of Haemonchus contortus after six years of levamisole usage. Research in Veterinary Science 47, 270–272.Google Scholar
Coles, G. C., Jackson, F., Pomroy, W. E., Prichard, R., von Samson-Himmelstjerna, G., Silvestre, A., Taylor, M. A. and Vercruysse, J. ( 2006). The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 136, 167–185. DOI: 10.1016/j.vetpar.2005.11.019CrossRefGoogle Scholar
Coles, G. and Stafford, K. A. ( 2000). Transmission of anthelmintic-resistant nematodes via hay? The Veterinary Record 147, 144.Google Scholar
Elard, L. ( 1998). La résistance aux benzimidazoles chez Teladorsagia circumcincta, nématode parasite de petits ruminants. Etude du déterminisme génétique et recherche des conséquences sur la fitness des parasites. Ph.D. thesis, Université François Rabelais, Tours.
Elard, L., Cabaret, J. and Humbert, J. F. ( 1999). PCR diagnosis of benzimidazole-susceptibility or -resistance in natural populations of the small ruminant parasite, Teladorsagia circumcincta. Veterinary Parasitology 80, 231–237. DOI: 10.1016/S0304-4017(98)00214-3CrossRefGoogle Scholar
Elard, L., Sauve, C. and Humbert, J. F. ( 1998). Fitness of benzimidazole-resistant and -susceptible worms of Teladorsagia circumcincta, a nematode parasite of small ruminants. Parasitology 117, 571–578. DOI: 10.1017/S0031182098003436CrossRefGoogle Scholar
Gaba, S., Cabaret, J., Ginot, V. and Silvestre, A. ( 2006). The early drug selection of nematodes to anthelmintics: stochastic transmission and population in refuge. Parasitology 133, 345–356. DOI: 10.1017/S0031182006000503CrossRefGoogle Scholar
Gruner, L., Elsen, J. M., Vu Tien Khang, J., Eychenne, F., Caritez, J. C., Jacquiet, P., Andreoletti, O., Sarradin, P., Cortet, J., Richer, N. and Leroux, H. ( 2004). Nematode parasites and scrapie: experiments in sheep and mice. Parasitology Research 93, 493–498. DOI: 10.1007/s00436-004-1131-7CrossRefGoogle Scholar
Hawley, D. M., Hanley, D., Dhondt, A. A. and Lovette, I. J. ( 2006). Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic. Molecular Ecology 15, 263–275. DOI: 10.1111/j.1365-294X.2005.02767.xCrossRefGoogle Scholar
Hubert, J., Kerboeuf, D. and Gruner, L. ( 1978). Epidemiology of gastro-intestinal nematode infections in sheep in a Limousin flock. Bulletin des Groupements Techniques Vétérinaires 1–16.Google Scholar
Kaplan, R. M. ( 2004). Drug resistance in nematodes of veterinary importance: a status report. Trends in Parasitology 20, 477–481. DOI: 10.1016/j.pt.2004.08.001CrossRefGoogle Scholar
Kerboeuf, D. ( 1985). Winter survival of trichostrongyle larvae: a study using tracer lambs. Research in Veterinary Science 38, 364–367.Google Scholar
Kerboeuf, D., Blackhall, W., Kaminsky, R. and 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. DOI: 10.1016/S0924-8579(03)00221-8CrossRefGoogle Scholar
Kwa, M. S. G., Okoli, M. N., Schulz-Key, H., Okongkwo, P. O. and Roos, M. H. ( 1998). Research note. Use of P-glycoprotein gene probes to investigate anthelmintic resistance in Haemonchus contortus and comparison with Onchocerca volvulus. International Journal for Parasitology 28, 1235–1240. DOI: 10.1016/S0020-7519(98)00071-XCrossRefGoogle Scholar
Leignel, V. ( 2000). Diversité génétique et résistance aux benzimidazoles chez Teladorsagia circumcincta (Nematoda, Trichostrongylidae), parasite de petits ruminants. Ph.D. thesis, Université, Montpellier II, Montpellier.
Leignel, V., Cabaret, J. and Humbert, J. F. ( 2002). New molecular evidence that Teladorsagia circumcincta (Nematoda: Trichostrongylidea) is a species complex. Journal of Parasitology 88, 135–140. DOI: 10.1645/0022-3395(2002)088[0135:NMETTC]2.0.CO;2CrossRefGoogle Scholar
Martin, P. J., Anderson, N. and Jarrett, R. G. ( 1989). Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays. Australian Veterinary Journal 66, 236–240.CrossRefGoogle Scholar
Mejia, M. E., Belisario, M., Fernandez, I., Schmidt, E. E. and Cabaret, J. ( 2003). Multispecies and multiple anthelmintic resistance on cattle nematodes in a farm in Argentina: the beginning of high resistance? The Veterinary Research 34, 461–467. DOI: 10.1051/vetres:2003018CrossRefGoogle Scholar
Peladeau, N. and Lacouture, Y. ( 1993). Simstat: Bootstrap computer simulation and statistical programm for IBM personal computers. Behavioral Research Methods, Instruments and Computers 25, 410–413.CrossRefGoogle Scholar
Raymond, M. ( 1985). Présentation d'un programme “Basic” d'analyse log-probit pour micro-ordinateur. Cahier ORSTOM Série Entomologie Médicale et Parasitologie 23, 117–121.Google Scholar
Rossanigo, C. E. and Gruner, L. ( 1995). Moisture and temperature requirements in faeces for the development of free-living stages of gastrointestinal nematodes of sheep, cattle and deer. Journal of Helminthology 69, 357–362.CrossRefGoogle Scholar
Silvestre, A., Chartier, C., Sauve, C. and Cabaret, J. ( 2000). Relationship between helminth species diversity, intensity of infection and breeding management in dairy goats. Veterinary Parasitology 94, 91–105. DOI 10.1016/S0304-4017(00)00367-8CrossRefGoogle Scholar
Silvestre, A. and Cabaret, J. ( 2002). Mutation in position 167 of isotype 1 β-tubulin gene of Trichostrongylid nematodes: role in benzimidazole resistance? Molecular and Biochemical Parasitology 120, 297–300. DOI: 10.1016/S0166-6851(01)00455-8CrossRefGoogle Scholar
Sissay, M. M., Asefa, A., Uggla, A. and Waller, P. J. ( 2006). Anthelmintic resistance of nematode parasites of small ruminants in eastern Ethiopia: Exploitation of refugia to restore anthelmintic efficacy. Veterinary Parasitology 135, 337–346. DOI: 10.1016/j.vetpar.2005.09.005CrossRefGoogle Scholar
Wyk, J. A. v. and Malan, F. S. ( 1988). Resistance of field strains of Haemonchus contortus to ivermectin, closantel, rafoxanide and the benzimidazoles in South Africa. Veterinary Record 123, 226–228.Google Scholar
Wyk, J. A. v. and van Schalkwyk, P. C. ( 1990). A novel approach to the control of anthelmintic-resistant Haemonchus contortus in sheep. Veterinary Parasitology 35, 61–69. DOI: 10.1016/0304-4017(90)90116-SCrossRefGoogle Scholar