Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T11:21:23.728Z Has data issue: false hasContentIssue false
  • English
  • Français

Modelling the short- and long-term impacts of drenching frequency and targeted selective treatment on the performance of grazing lambs and the emergence of anthelmintic resistance

Published online by Cambridge University Press:  01 February 2013

YAN C. S. M. LAURENSON ,
STEPHEN C. BISHOP ,
ANDREW B. FORBES  and
ILIAS KYRIAZAKIS
YAN C. S. M. LAURENSON*
Affiliation:
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian EH25 9RG, UK
STEPHEN C. BISHOP
Affiliation:
The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian EH25 9RG, UK
ANDREW B. FORBES
Affiliation:
Merial, 29 avenue Tony Garnier, Lyon 69007, France
ILIAS KYRIAZAKIS
Affiliation:
School of Agriculture, Food and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
*
*Corresponding author: The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian EH25 9RG, UK. Tel: +44 131 651 9100. Fax: +44 131 651 9105. E-mail: yan.laurenson@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Refugia-based treatment strategies aim to prolong anthelmintic efficacy by maintaining a parasite population unexposed to anthelmintics. Targeted selective treatment (TST) achieves this by treating only animals that will benefit most from treatment, using a determinant criterion (DC). We developed a mathematical model to compare various traits proposed as DC, and investigate impacts of TST and drenching frequency on sheep performance and anthelmintic resistance. Short term, decreasing the proportion of animals drenched reduced benefits of anthelmintic treatment, assessed by empty body weight (EBW), but decreased the rate of anthelmintic resistance development; each consecutive drenching had a reduced impact on average EBW and an increased impact on the rate of anthelmintic resistance emergences. The optimal DC was fecal egg count, maintaining the highest average EBW when reducing the proportion of animals drenched. Long-term, reducing the proportion of animals drenched had little impact on total weight gain benefits, across animals and years, whilst reducing drenching frequency increased it. Decreasing the frequency and proportion of animals drenched were both predicted to increase the duration of anthelmintic efficacy but reduce the total number of drenches administered before resistance was observed. TST and frequency of drenching may lead to different benefits in the short versus long term.

Keywords

anthelmintic resistancerefugiasheepsimulation modellingtargeted selective treatmentTeladorsagia circumcincta
Type
Research Article
Information
Parasitology , Volume 140 , Issue 6 , May 2013 , pp. 780 - 791
Copyright
Copyright © Cambridge University Press 2013

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

AFRC (1993). Energy and Protein Requirements of Ruminants. An advisory manual prepared by AFRC Technical Committee on Responses to Nutrients. CAB International, Wallingford, UK.Google 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)80117-0.CrossRefGoogle ScholarPubMed
Barrett, M., Jackson, F. and Huntley, J. F. (1998). Pathogenicity and immunogenicity of different isolates of Teladorsagia circumcincta. Veterinary Parasitology 76, 95–104. doi: 10.1016/S0304-4017(97)00221-5.CrossRefGoogle ScholarPubMed
Besier, R. B. (2007). New anthelmintics for livestock: the time is right. Trends in Parasitology 23, 21–24. doi: 10.1016/j.pt.2006.11.004.CrossRefGoogle ScholarPubMed
Besier, R. B. (2012). Refugia-based strategies for sustainable worm control: factors affecting the acceptability to sheep and goat owners. Veterinary Parasitology 186, 2–9. doi: 10.1016/j.vetpar.2011.11.057.CrossRefGoogle ScholarPubMed
Bishop, S. C., Bairden, K., McKellar, Q. A., Park, M. and Stear, M. J. (1996). Genetic parameters for faecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with live weight in young lambs. Animal Science 63, 423–428. doi: 10.1017/S1357729800015319.CrossRefGoogle Scholar
Bishop, S. C. and Stear, M. J. (1997). Modelling responses to selection for resistance to gastro-intestinal parasites in sheep. Animal Science 64, 469–478. doi: 10.1017/S135772980015319CrossRefGoogle Scholar
Borgsteede, F. H. M. (1993). The efficacy and persistent anthelmintic effect of ivermectin in sheep. Veterinary Parasitology 50, 117–124. doi: 10.1016/0304-4017(93)90012-C.CrossRefGoogle ScholarPubMed
Cammack, K. M., Leymaster, K. A., Jenkins, T. G. and Nielsen, M. K. (2005). Estimates of genetic parameters for food intake, feeding behavior, and daily gain in composite ram lambs. Journal of Animal Science 83, 777–785.CrossRefGoogle ScholarPubMed
Coles, G. C. (2005). Anthelmintic resistance – looking to the future: a UK perspective. Research in Veterinary Science 78, 99–108. doi: 10.1016/j.rvsc.2004.09.001CrossRefGoogle Scholar
Coles, G. C., Bauer, C., Borgsteede, F. H. M., Geerts, S., Klei, T. R., Taylor, M. A. and Waller, P. J. (1992). World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 44, 35–44. doi: 10.1016/0304-4017(92)90141-U.CrossRefGoogle ScholarPubMed
Coop, R. L., Graham, R. B., Jackson, F., Wright, S. E. and Angus, K. W. (1985). Effect of experimental Ostertagia circumcincta infection on the performance of grazing lambs. Research in Veterinary Science 38, 282–287.CrossRefGoogle ScholarPubMed
Coop, R. L., Sykes, A. R. and Angus, K. W. (1982). The effect of three levels of intake of Ostertagia circumcincta larvae on growth rate, feed intake and body composition of growing lambs. Journal of Agricultural Science 98, 247–255. doi: 10.1017/S0021859600041782CrossRefGoogle Scholar
Cringoli, G., Rinaldi, L., Veneziano, V., Mezzino, L., Vercruysse, J. and Jackson, F. (2009). Evaluation of targeted selected treatments in sheep in Italy: effects of faecal worm egg count and milk production in four case studies. Veterinary Parasitology 164, 36–43. doi: 10.1016/j.vetpar.2009.04.010.CrossRefGoogle ScholarPubMed
Dobson, R. L., Barnes, E. H., Tyrrell, K. L., Hosking, B. C., Larsen, J. W. A., Besier, R. B., Love, S., Rolfe, P. F. and Bailey, J. N. (2011). A multi-species model to assess the effect of refugia on worm control and anthelmintic resistance in sheep grazing systems. Australian Veterinary Journal 89, 200–208. doi: 10.1111/j.1751-0813.2011.00719.x.CrossRefGoogle ScholarPubMed
Doeschl_Wilson, A. B., Vagenas, D., Kyriazakis, I. and Bishop, S. C. (2008). Challenging the assumptions underlying genetic variation in host nematode resistance. Genetics, Selection, Evolution 40, 241–264. doi: 10.1051/gse:2008001.Google Scholar
Elard, L. and Humbert, J. F. (1999). Importance of the mutation of amino acid 200 of the isotype 1 β-tubulin gene in the benzimidazole resistance of the small-ruminant parasite Teladorsagia circumcincta. Parasitology Research 85, 452–456. doi: 10.1007/s004360050577.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Gaba, S., Cabaret, J., Sauvé, C., Cortet, J. and Silvestre, A. (2010). Experimental and modelling approaches to evaluate different aspects of the efficiency of targeted selective treatment of anthelmintics against sheep parasite nematodes. Veterinary Parasitology 171, 254–262. doi: 10.1016/j.vetpar.2010.03.040.CrossRefGoogle ScholarPubMed
Gallidis, E., Papadopoulos, E., Ptochos, S. and Arsenos, G. (2009). The use of targeted selective treatments against gastrointestinal nematodes in milking sheep and goats in Greece based on parasitological and performance criteria. Veterinary Parasitology 164, 53–58. doi: 10.1016/j.vetpar.2009.04.011.CrossRefGoogle ScholarPubMed
Gibson, T. E. and Everett, G. (1972). The ecology of the free-living stages of Ostertagia circumcincta. Parasitology 64, 451–460. doi: 10.1017/S0031182000045522.CrossRefGoogle ScholarPubMed
Gilleard, J. S. (2006). Understanding anthelmintic resistance: the need for genomics and genetics. International Journal for Parasitology 36, 1227–1239. doi: 10.1016/j.ijpara.2006.06.010.CrossRefGoogle ScholarPubMed
Greer, A. W., Huntley, J. F., Mackellar, A., McAnulty, R. W., Jay, N. P., Green, R. S., Stankiewicz, M. and Sykes, A. R. (2008). The effect of corticosteroid treatment on local immune responses, intake and performance in lambs infected with Teladorsagia circumcincta. International Journal for Parasitology 38, 1717–1728. doi: 10.1016/j.ijpara.2008.05.010.CrossRefGoogle ScholarPubMed
Hoste, H., Le Frileux, Y. and Pommaret, A. (2001). Distribution and repeatability of faecal egg counts and blood parameters in dairy goats naturally infected with gastrointestinal nematodes. Research in Veterinary Science 70, 57–60. doi: 10.1053/rvsc.2000.0442.CrossRefGoogle ScholarPubMed
Jabbar, A., Iqbal, Z., Kerboeuf, D., Muhammad, G., Khan, M. N. and Afaq, M. (2006). Anthelmintic resistance: the state of play revisited. Life Sciences 79, 2413–2431. doi: 10.1016/j.lfs.2006.08.010.CrossRefGoogle ScholarPubMed
Jackson, F. and Coop, R. L. (2000). The development of anthelmintic resistance in sheep nematodes. Parasitology 120, S95–S107.CrossRefGoogle ScholarPubMed
Jackson, F. and Waller, P. J. (2008). Managing refugia. Tropical Biomedicine 25, 34–40.Google ScholarPubMed
Jenkins, S. J. and Allen, J. E. (2010). Similarity and diversity in macrophage activation by nematodes, trematodes, and cestodes. Journal of Biomedicine and Biotechnology. doi: 10.1155/2010/262609.CrossRefGoogle ScholarPubMed
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.2004.08.001.CrossRefGoogle ScholarPubMed
Kenyon, F., Greer, A. W., Coles, G. C., Cringoli, G., Papadopoulos, E., Cabaret, J., Berrag, B., Varady, M., van Wyk, J. A., Thomas, E., Vercruysse, J. and Jackson, F. (2009). The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants. Veterinary Parasitology 164, 3–11. doi: 10.1016/j.vetpar.2006.04.015.CrossRefGoogle Scholar
Kenyon, F. and Jackson, F. (2012). Targeted flock/herd and individual ruminant treatment approaches. Veterinary Parasitology 186, 10–17. doi: 10.1016/j.vetpar.2011.041.CrossRefGoogle ScholarPubMed
Kyriazakis, I. (2010). Is anorexia during infection in animals affected by food composition? Animal Feed Science and Technology 156, 1–9. doi: 10.1016/j.anifeedsci.2010.01001.CrossRefGoogle Scholar
Laurenson, Y. C. S. M., Bishop, S. C. and Kyriazakis, I. (2011). In silico exploration of the mechanisms that underlie parasite-induced anorexia in sheep. British Journal of Nutrition 106, 1023–1039. doi: 10.1017/S0007114511001371.CrossRefGoogle ScholarPubMed
Laurenson, Y. C. S. M., Kyriazakis, I. and Bishop, S. C. (2012 a). In silico exploration of the impact of pasture contamination and anthelmintic treatment on genetic parameter estimates for parasite resistance in grazing sheep. Journal of Animal Science 90, 2167–2180. doi: 10.2527/jas.2011–4527.CrossRefGoogle ScholarPubMed
Laurenson, Y. C. S. M., Kyriazakis, I., Forbes, A. B. and Bishop, S. C. (2012 b). Exploration of the epidemiological consequences of resistance to gastro-intestinal parasitism and grazing management of sheep through a mathematical model. Veterinary Parasitology 189, 238–249. doi: 10.1016/j.vetpar.2012.05.005.CrossRefGoogle ScholarPubMed
Learmount, J., Taylor, M. A., Smith, G. and Morgan, C. (2006). A computer model to simulate control of parasitic gastroenteritis in sheep on UK farms. Veterinary Parasitology 142, 312–329. doi: 10.1016/j.vetpar.2006.07.012.CrossRefGoogle ScholarPubMed
Leathwick, D. M. (2012). Modelling the benefits of a new class of anthelmintic in combination. Veterinary Parasitology 186, 93–100. doi: 10.1016/j.vetpar.2011.11.050.CrossRefGoogle ScholarPubMed
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)00059-3.CrossRefGoogle Scholar
Leathwick, D. M., Waghorn, T. S., Miller, C. M., Atkinson, D. S., Haack, N. A. and Oliver, A-M. (2006 a). Selective and on demand drenching of lambs: impact on parasite populations and performance of lambs. New Zealand Veterinary Journal 54, 305–312. doi: 10.1080/00480169.2006.36715.CrossRefGoogle ScholarPubMed
Leathwick, D. M., Miller, C. M., Atkinson, D. S., Haack, N. A., Alexander, R. A., Oliver, A-M., Waghorn, T. S., Potter, J. F., Sutherland, I. A. (2006 b). Drenching adult ewes: implications of anthelmintic treatments pre- and post-lambing on the development of anthelmintic resistance. New Zealand Veterinary Journal 54, 297–304. doi: 10.1080/00480169.2006.36714.CrossRefGoogle ScholarPubMed
Leathwick, D. M., Hosking, B. C., Bisset, S. A. and McKay, C. H. (2009). Managing anthelmintic resistance: is it feasible in New Zealand to delay the emergence of resistance to a new anthelmintic class? New Zealand Veterinary Journal 57, 181–192. doi: 10.1080/00480169·2009·36900.CrossRefGoogle ScholarPubMed
Leignel, V. and Cabaret, J. (2001). Massive use of chemotherapy influences life traits of parasitic nematodes in domestic ruminants. Functional Ecology 15, 569–574. doi: 10.1046/j.0269-8463.2001.00567.x.CrossRefGoogle Scholar
Louie, K., Vlassoff, A. and Mackay, A. (2005). Nematode parasites of sheep: extension of a simple model to include host variability. Parasitology 130, 437–446. doi: 10.1017/S003118200400678X.CrossRefGoogle ScholarPubMed
Morgan, E. R. and van Dijk, J. (2012). Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe. Veterinary Parasitology 189, 8–14. doi: 10.1016/j.vetpar.2012.03.028.CrossRefGoogle ScholarPubMed
Nielsen, M. K., Kaplan, R. M., Thamsborg, S. M., Monrad, J. and Olsen, S. N. (2007). Climatic influences on development and survival of free-living stages of equine strongyles: implications for worm control strategies and managing anthelmintic resistance. Veterinary Journal 174, 23–32. doi: 10.1016/j.tvjl.2006.05.009.CrossRefGoogle ScholarPubMed
Papadopoulos, E. (2008). Anthelmintic resistance in sheep nematodes. Small Ruminant Research 76, 99–103. doi: 10.1016/j.smallrumres.2007.12.012.CrossRefGoogle Scholar
Papadopoulos, E., Gallidis, E. and Ptochos, S. (2012). Anthelmintic resistance in sheep in Europe : a selected review. Veterinary Parasitology 189, 85–88. doi: 10.1016/j.vetpar.2012.03.036.CrossRefGoogle ScholarPubMed
Sargison, N. D., Jackson, F., Bartley, D. J., Wilson, D. J., Stenhouse, L. J. and Penny, C. D. (2007). Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the south-east of Scotland. Veterinary Parasitology 145, 65–76. doi: 10.1016/j.vetpar.2006.10.024.CrossRefGoogle ScholarPubMed
Sibbald, A. M., Shellard, L. J. F. and Smart, T. S. (2000). Effects of space allowance on the grazing behaviour and spacing of sheep. Applied Animal Behaviour Science 70, 49–62. doi: 10.1016/S0168-1591(00)00145-3.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Soulsby, L. (2007). New concepts in strongyle control and anthelmintic resistance: the role of refugia. Veterinary Journal 174, 6–7.CrossRefGoogle ScholarPubMed
Sreter, T., Molnar, V. and Kassai, T. (1994). The distribution of nematode egg counts and larval counts in grazing sheep and their implications for parasite control. International Journal for Parasitology 24, 103–108. doi: 10.1016/0020-7519(94)90063-9.CrossRefGoogle ScholarPubMed
Stafford, K. A., Morgan, E. R. and Coles, G. C. (2009). Weight-based targeted selected treatment of gastrointestinal nematodes in a commercial sheep flock. Veterinary Parasitology 164, 59–65. doi: 10.1016/j.vetpar.2009.04.009.CrossRefGoogle Scholar
Stear, M. J., Boag, B., Cattadori, I. and Murphy, L. (2009). Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infection of sheep: from heritabilities to gene identification. Parasite Immunology 31, 274–282. doi: 10.1111/j.1365-3024.2009.01105.x.CrossRefGoogle ScholarPubMed
Torres-Acosta, J. F. J. and Hoste, H. (2008). Alternative or improved methods to limit gastro-intestinal parasitism in grazing sheep and goats. Small Ruminant Research 77, 159–173. doi: 10.1016/j.smallrumres.2008.03.009.CrossRefGoogle Scholar
Vagenas, D., Bishop, S. C. and Kyriazakis, I. (2007). A model to account for the consequences of host nutrition on the outcome of gastrointestinal parasitism in sheep: logic and concepts. Parasitology 134, 1263–1277. doi: 10.1017/S0031182007002624.CrossRefGoogle Scholar
van Wyk, J. A. (2001). Refugia – overlooked as perhaps the most important factor concerning the development of anthelmintic resistance. Onderstepoort Journal of Veterinary Research 68, 55–67.Google ScholarPubMed
van Wyk, J. A., Hoste, H., Kaplan, R. M. and Besier, R. B. (2006). Targeted selective treatment for worm management – how do we sell rational programs to farmers? Veterinary Parasitology 139, 336–346. doi: 10.1016/j.vetpar.2006.04·023.CrossRefGoogle ScholarPubMed
Waghorn, T. S., Leathwick, D. M., Miller, C. M. and Atkinson, D. S. (2008). Brave or gullible: testing the concept that leaving susceptible parasites in refugia will slow the development of anthelmintic resistance. New Zealand Veterinary Journal 56, 158–163. doi: 10.1080/00480169.2008.36828.CrossRefGoogle ScholarPubMed
Waller, P. J. (2006). From discovery to development: current industry perspectives for the development of novel methods of helminth control in livestock. Veterinary Parasitology 139, 1–14. doi: 10.1016/j.vetpar.2006.02.036.CrossRefGoogle ScholarPubMed
Wolstenholme, A. J., Fairweather, I., Pritchard, R., Von Samson-Himmelstjerna, G. and Sangster, N. C. (2004). Drug resistance in veterinary helminths. Trends in Parasitology 20, 469–476. doi: 10.1016/j.pt.2004.07.010.CrossRefGoogle ScholarPubMed
Yakoob, A. Y., Holmes, P. H., Parkins, J. J. and Armour, J. (1983). Plasma protein loss associated with gastrointestinal parasitism in grazing sheep. Research in Veterinary Science 34, 58–63.CrossRefGoogle ScholarPubMed
Young, R. R., Anderson, N., Overend, D., Tweedie, R. L., Malafant, K. W. J. and Preston, G. A. N. (1980). The effect of temperature on times to hatching of eggs of the nematode Ostertagia circumcincta. Parasitology 81, 477–491. doi: 10.1017/S0031182000061874.CrossRefGoogle ScholarPubMed