Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-20T06:44:26.003Z Has data issue: false hasContentIssue false
  • English
  • Français

The early drug selection of nematodes to anthelmintics: stochastic transmission and population in refuge

Published online by Cambridge University Press:  09 June 2006

S. GABA ,
J. CABARET ,
V. GINOT  and
A. SILVESTRE
S. GABA
Affiliation:
INRA, Research Unit Biometry, Domaine Saint-Paul – Site Agroparc 84914 Avignon Cedex 9, France INRA, Research Unit Animal Infectious Diseases and Public Health, 37380 Nouzilly, France
J. CABARET
Affiliation:
INRA, Research Unit Animal Infectious Diseases and Public Health, 37380 Nouzilly, France
V. GINOT
Affiliation:
INRA, Research Unit Biometry, Domaine Saint-Paul – Site Agroparc 84914 Avignon Cedex 9, France
A. SILVESTRE
Affiliation:
INRA, Research Unit Animal Infectious Diseases and Public Health, 37380 Nouzilly, France
Get access Rights & Permissions [Opens in a new window]

Abstract

We have developed an individual-based model to reflect the complexity of the early phase of drug resistance selection in a nematode/sheep model. The infection process consists of the stochastic ingestion of infective larvae spatially aggregated in clumps. Each clump corresponds to infective larvae, which are the offspring of the mature nematodes from a given sheep. We studied the dynamics of the parasitic population and the frequency of the recessive resistance alleles during selection by anthelmintic treatments. The interaction between genetic and demographic processes illustrated the trade-off between the control of the infection and the delay of resistance selection. We confirmed the importance of the number of treatments and their timing. The same treatment frequency may result in different outcomes on resistance selection in relation to the size of the refuge (infective larvae on pasture). Treatment applied during the summer (when the mortality of infective larvae on pasture was high), may lead to a rapid selection of drug resistance and a lack of control of sheep and pasture contamination. We showed that higher stocking rates were also a force in promoting the resistance allele selection.

Keywords

population dynamicsdrug resistancestochastic modelnematode parasitesheeprefuge
Type
Research Article
Information
Parasitology , Volume 133 , Issue 3 , September 2006 , pp. 345 - 356
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aumont, G., Gauthier, D., Gruner, L. and Matheron, G. ( 1992). Dynamics of the free-living populations of gastrointestinal trichostrongyles of cattle in a natural grazing system in Guadeloupe (French West Indies). Preventive Veterinary Medicine 12, 245–258. DOI: 10.1016/0167-5877(92)90053-ICrossRefGoogle Scholar
Barger, I. A. ( 1993). Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. International Journal for Parasitology 23, 463–469. DOI: 10.1016/0020-7519(93)90034-VCrossRefGoogle Scholar
Barnes, E. H., Dobson, R. J. and Barger, I. A. ( 1995). Worm control and anthelmintic resistance: adventures with a model. Parasitology Today 11, 56–63. DOI: 10.1016/0169-4758(95)80117-0CrossRefGoogle Scholar
Bishop, S. C. and Stear, M. J. ( 2000). The use of a gamma-type function to assess the relationship between the number of adult Teladorsagia circumcincta and total egg output. Parasitology 121, 435–440. DOI: 10.1017/S0031182099006526CrossRefGoogle Scholar
Cabaret, J., Mage, C. and Bouilhol, M. ( 2002). Helminth intensity and diversity in organic meat sheep farms in centre of France. Veterinary Parasitology 105, 33–47. DOI: 10.1016/S0304-4017(01)00647-1CrossRefGoogle Scholar
Cabaret, J. and Ouhelli, H. ( 1984). Fertility of parasitic strongyles in the digestive system of sheep under natural conditions. Revue de Médecine Vétérinaire 135, 627–633.Google Scholar
Chartier, C. and Reche, B. ( 1992). Gastrointestinal helminths and lungworms of French dairy goats: prevalence and geographical distribution in Poitou-Charentes. Veterinary Research Communications 16, 327–335. DOI: 10.1007/BF01839182CrossRefGoogle Scholar
Cornell, S. J., Isham, V. S. and Grenfell, B. T. ( 2004). Stochastic and spatial dynamics of nematode parasites in farmed ruminants. Proceedings of the Royal Society of London, B 271, 1243–1250. DOI: 10.1098/rspb.2004.2744CrossRefGoogle Scholar
Cornell, S. J., Isham, V. S., Smith, G. and Grenfell, B. T. ( 2003). Spatial parasite transmission, drug resistance, and the spread of rare genes. Proceedings of the National Academy of Sciences, USA 100, 7401–7405. DOI: 10.1073/pnas.0832206100CrossRefGoogle Scholar
Criscione, C. D. and Blouin, M. S. ( 2005). Effective sizes of macroparasite populations: a conceptual model. Trends in Parasitology 21, 212–217. DOI: 10.1016/j.pt.2005.03.002CrossRefGoogle Scholar
Dobson, R. J., Griffiths, D. A., Donald, A. D. and Waller, P. J. ( 1987). A genetic model describing the evolution of levamisole resistance in Trichostrongylus colubriformis, a nematode parasite of sheep. IMA Journal of Mathematics Applied in Medicine and Biology 4, 279–293.CrossRefGoogle Scholar
Dobson, R. J., Waller, P. J. and Donald, A. D. ( 1990 a). Population dynamics of Trichostrongylus colubriformis in sheep: the effect of host age on the establishment of infective larvae. International Journal for Parasitology 20, 353–357. DOI: 10.1016/0020-7519(90)90151-CCrossRefGoogle Scholar
Dobson, R. J., Waller, P. J. and Donald, A. D. ( 1990 b). Population dynamics of Trichostrongylus colubriformis in sheep: the effect of infection rate on loss of adult parasites. International Journal for Parasitology 20, 359–363. DOI: 10.1016/0020-7519(90)90150-LCrossRefGoogle Scholar
Donald, A. D. and Waller, P. J. ( 1973). Gastro-intestinal nematode parasite populations in ewes and lambs and the origin and time course of infective larval availability in pastures. International Journal for Parasitology 3, 219–233.CrossRefGoogle Scholar
Elard, L. and Humbert, J. F. ( 1999). Importance of the mutation of amino acid 200 of the isotype 1 beta -tubulin gene in the benzimidazole resistance of the small-ruminant parasite Teladorsagia circumcincta. Parasitology Research 85, 452–456. DOI: 10.1007/s004360050577CrossRefGoogle Scholar
Euzeby, J., Gevrey, J. and Moraillon, P. ( 1964). Evolution du parasitisme helminthique dans un troupeau d'ovins: Synthèse des observations de trois années (1961 à 1964). Revue de Médecine Vétérinaire 10, 629–643.Google Scholar
Gaba, S., Ginot, V. and Cabaret, J. ( 2005). Modelling macroparasite aggregation using a nematode-sheep system: the Weibull distribution as an alternative to the Negative Binomial distribution? Parasitology 131, 393–401. DOI: 10.1017/S003118200500764XCrossRefGoogle Scholar
Gettinby, G. ( 1989). Computational veterinary parasitology with an application to chemical resistance. Veterinary Parasitology 32, 57–72. DOI: 10.1016/0304-4017(89)90155-6CrossRefGoogle Scholar
Grenfell, B. T., Smith, G. and Anderson, R. M. ( 1987). A mathematical model of the population biology of Ostertagia ostertagi in calves and yearlings. Parasitology 95, 389–406.CrossRefGoogle Scholar
Guesdon, J. C. ( 2003). Round Table: Common Agricultural Policy of the European Union. Analysis in the sheep sector. In Colloquium of the European Union, Paris, France, 7 Décembre 2003. Available on 4 March 2006 at: http://www.inst-elevage.asso.fr/html1/article.php3?id_article=6055&origine=49.
Hansen, J. W., Nansen, P. and Foldager, J. ( 1980). The importance of stocking rate to the uptake of gastrointestinal nematodes by grazing calves. In Epidemiology and Control of Nematodiasis in Cattle. An Animal Pathology Workshop in the CEC Programme of Coordination of Agricultural Research, Royal Veterinary and Agricultural University, Copenhagen, Denmark9, 471–494.
Hong, C., Hunt, K. R. and Coles, G. C. ( 1996). Occurrence of anthelmintic resistant nematodes on sheep farms in England and goat farms in England and Wales. Veterinary Record 139, 83–86.CrossRefGoogle 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
Leathwick, D. M., Vlassoff, A. and Barlow, N. D. ( 1995). A model for nematodiasis in New Zealand lambs: the effect of drenching regime and grazing management on the development of anthelmintic resistance. International Journal for Parasitology 25, 1479–1490. DOI: 10.1016/0020-7519(95)00059-3CrossRefGoogle Scholar
Lenormand, T. and Raymond, M. ( 1998). Resistance management: the stable zone strategy. Proceedings of the Royal Society of London, B 265, 1985–1990. DOI: 10.1098/rspb.1998.0529CrossRefGoogle Scholar
Mangeon, N. ( 1986). Epizootiology of gastro-intestinal and pulmonary parasites of goats in Touraine. Periods and areas of high risk. Thesis, Ecole Nationale Supérieure Agronomique de Montpellier, France.Google Scholar
May, R. M. ( 1977). Togetherness among schistosomes: its effects on the dynamics of the infection. Mathematical Biosciences 35, 301–343.CrossRefGoogle Scholar
Mehlhorn, H. ( 2001). Nematocidal drugs. In Encyclopedic Reference of Parasitology: Diseases, Treatment, Therapy. Springer-Verlag, Berlin, Germany, pp. 363–447.CrossRef
Paterson, S. and Viney, M. E. ( 2000). The interface between epidemiology and population genetics. Parasitology Today 16, 528–532. DOI: 10.1016/S0169-4758(00)01776-2CrossRefGoogle Scholar
Poulin, R. ( 1998). Evolutionary Ecology of Parasites: from Individuals to Communities. Chapman and Hall Ltd, London, UK.
Saul, A. ( 1995). Computer model of the maintenance and selection of genetic heterogeneity in polygamous helminths. Parasitology 111, 531–536.CrossRefGoogle Scholar
Saulai, M., Cabaret, J., Hostache, G., Mandonnet, N. and Aumont, G. ( 2001). Life-trait evolution of a parasite strongyle nematode in response to host resistance: an experimental approach using Haemonchus contortus in black belly lambs. Genetics, Selection, Evolution 33, 25–44.Google Scholar
Shaw, D. J. and Dobson, A. P. ( 1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, 111–127.CrossRefGoogle Scholar
Smith, G. ( 1990). A mathematical model for the evolution of anthelmintic resistance in a direct life cycle nematode parasite. International Journal for Parasitology 20, 913–921. DOI: 10.1016/0020-7519(90)90030-QCrossRefGoogle Scholar
Smith, G. and Grenfell, B. T. ( 1985). The population biology of Ostertagia ostertagi. Parasitology Today 1, 76–81. DOI: 10.1016/0169-4758(85)90047-XCrossRefGoogle Scholar
Smith, G., Grenfell, B. T., Isham, V. and Cornell, S. ( 1999). Anthelmintic resistance revisited: under-dosing, chemoprophylactic strategies, and mating probabilities. International Journal for Parasitology 29, 77–91. DOI: 10.1016/S0020-7519(98)00186-6CrossRefGoogle Scholar
Tallis, G. M. and Leyton, M. ( 1969). Stochastic models of populations of helminthic parasites in the definitive host. Mathematical Biosciences 4, 39–48.CrossRefGoogle Scholar
Vacher, C., Bourguet, D., Rousset, F., Chevillon, C. and Hochberg, M. E. ( 2003). Modelling the spatial configuration of refuges for a sustainable control of pests: a case study of Bt cotton. Journal of Evolutionary Biology 16, 378–387. DOI: 10.1046/j.1420-9101.2003.00553.xCrossRefGoogle Scholar