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International journal for parasitology. Drugs and drug resistance2019; 10; 118-124; doi: 10.1016/j.ijpddr.2019.08.008

Managing anthelmintic resistance in cyathostomin parasites: Investigating the benefits of refugia-based strategies.

Abstract: Selective anthelmintic therapy has been recommended as a sustainable strategy for cyathostomin control in horse populations for several decades. The traditional approach has been to determine strongyle fecal egg counts (FEC) for all horses, with treatment only recommended for those exceeding a predetermined threshold. The aims are to achieve a reduction of overall egg shedding, while leaving a proportion of the herd untreated, which lowers anthelmintic treatment intensity and reduces selection pressure for development of anthelmintic resistance. This study made use of the cyathostomin model to evaluate the influence of treatment strategies with between 1 and 8 yearly treatment occasions, where either 1) all horses were treated, 2) a predetermined proportion of the herd remained untreated, or 3) horses were treated if their FEC exceeded thresholds between 100 and 600 strongyle eggs per gram. Weather data representing four different climatic zones was used and three different herd age structures were compared; 1) all yearlings, 2) all mature horses 10-20 years old, and 3) a mixed age structure of 1-20 years of age. Results indicated a consistent effect of age structure, with anthelmintic resistance developing quickest in the yearling group and slowest among the mature horses. Development of anthelmintic resistance was affected by treatment intensity and selective therapy generally delayed resistance. Importantly, the results suggest that the effects of selective therapy on resistance development are likely to vary between climatic zones and herd age structures. Overall, a substantial delaying of resistance development requires that the average number of treatments administered annually across a herd of horses needs to be about two or less. However, results also indicate that an age-structured prioritisation of treatment to younger horses should still be effective. It appears that a 'one-size-fits-all' approach to the management of anthelmintic resistance in cyathostomins is unlikely to be optimal.
Publication Date: 2019-08-28 PubMed ID: 31491731PubMed Central: PMC6731328DOI: 10.1016/j.ijpddr.2019.08.008Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research study assesses the impact of different treatment strategies on managing anthelmintic resistance in cyathostomin parasites. The study showed that factors such as climate, herd age, and treatment frequency influence resistance development, and no one method suits all situations.

Study Method

  • The researchers used a cyathostomin model to investigate the effects of various treatment strategies for horse populations affected by cyathostomin parasites. Commonly, anthelmintic therapy is administered to horses with strongyle fecal egg counts (FEC) above a certain threshold, leaving some of the population untreated, thereby reducing the likelihood of anthelmintic resistance.
  • The study assessed 1 to 8 yearly treatment strategies, where either all horses were treated, a part of the herd remained untreated, or horses were treated if their FEC exceeded thresholds between 100 and 600 eggs per gram.
  • Different climatic zones were accounted for by utilizing weather data from four distinct areas. The study also evaluated three age groups, including all yearlings, all mature horses aged 10-20, and a mixed age structure of horses aged 1-20 years.

Results and Findings

  • The study found that the development of anthelmintic resistance is influenced by the intensity of treatment and the age structure of the horse population. Resistance developed faster in the group of yearlings and slower among mature horses.
  • Across different climatic zones and herd age structures, selective therapy generally helped delay resistance, although the effect varies.
  • The results suggested, to significantly delay the development of resistance, the average number of treatments across a herd needs to be about two or fewer per year. An age-structured prioritisation of treatment, particularly focussing on younger horses, seems to be effective.
  • The study indicates that a ‘one-size-fits-all’ approach to managing anthelmintic resistance in cyathostomin parasites is unlikely to be the most effective strategy due to varying factors.

Study Implications

  • The findings highlight that multiple facets like climate, age structure of the herd, and treatment intensity must be considered when formulating strategies to manage anthelmintic resistance in cyathostomin-infected horse populations.
  • In conclusion, individualized plans based on the specific circumstances and conditions of each herd appear to be the key to successful and sustainable anthelmintic resistance management, rather than a singular, blanket approach.

Cite This Article

APA
Leathwick DM, Sauermann CW, Nielsen MK. (2019). Managing anthelmintic resistance in cyathostomin parasites: Investigating the benefits of refugia-based strategies. Int J Parasitol Drugs Drug Resist, 10, 118-124. https://doi.org/10.1016/j.ijpddr.2019.08.008

Publication

ISSN: 2211-3207
NlmUniqueID: 101576715
Country: Netherlands
Language: English
Volume: 10
Pages: 118-124

Researcher Affiliations

Leathwick, Dave M
  • AgResearch, Grasslands Research Centre, Private Bag 11008, Palmerston North, 4442, New Zealand. Electronic address: dave.leathwick@agresearch.co.nz.
Sauermann, Christian W
  • AgResearch, Grasslands Research Centre, Private Bag 11008, Palmerston North, 4442, New Zealand.
Nielsen, Martin K
  • M.H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, USA.

MeSH Terms

  • Age Factors
  • Animals
  • Anthelmintics / administration & dosage
  • Drug Resistance
  • Feces / parasitology
  • Female
  • Horses
  • Male
  • Parasite Egg Count
  • Refugium
  • Strongyle Infections, Equine / drug therapy
  • Strongyle Infections, Equine / parasitology
  • Strongylida / drug effects
  • Strongylida / physiology

References

This article includes 39 references
  1. Barnes E.H., Dobson R.J., Barger I.A.. Worm control and anthelmintic resistance: adventures with a model.. Parasitol. Today 1995;11:56–63.
    pubmed: 15275374
  2. Becher A.M., van Doorn D.C., Pfister K., Kaplan R.M., Reist M., Nielsen M.K.. Equine parasite control and the role of national legislation - a multinational questionnaire survey.. Vet. Parasitol. 2018;259:6–12.
    pubmed: 30056985
  3. Boersema J.H., Eysker M., Maas J., van der Aar W.M.. Comparison of the reappearance of strongyle eggs in foals, yearlings, and adult horses after treatment with ivermectin or pyrantel.. Vet. Q. 1996;18:7–9.
    pubmed: 8833604
  4. Chapman M.R., French D.D., Klei T.R.. Prevalence of strongyle nematodes in naturally infected ponies of different ages and during different seasons of the year in Louisiana.. J. Parasitol. 2003;89:309–314.
    pubmed: 12760645
  5. Dobson R.J., Waller P.J., Donald A.D.. Population dynamics of Trichostrongylus colubriformis in sheep: the effect of infection rate on loss of adult parasites.. Int. J. Parasitol. 1990;2:359–363.
    pubmed: 2358319
  6. Duncan J.L., Love S.. Preliminary observations on an alternative strategy for the control of horse strongyles.. Equine Vet. J. 1991;23:226–228.
    pubmed: 1909236
  7. Geurden T., van Doorn D., Claerebout E., Kooyman F., De Keersmaecker S., Vercruysse J., Besognet B., Vanimisetti B., di Regalbono A.F., Beraldo P., Di Cesare A., Traversa D.. Decreased strongyle egg re-appearance period after treatment with ivermectin and moxidectin in horses in Belgium, Italy and The Netherlands.. Vet. Parasitol. 2014;204:291–296.
    pubmed: 24880643
  8. Gomez H.H., Georgi J.R.. Equine helminth infections: control by selective chemotherapy.. Equine Vet. J. 1991;23:198–200.
    pubmed: 1884701
  9. Hodgkinson J.E., Kaplan R.M., Kenyon F., Morgan E.R., Park A.W., Paterson S., Babayan S.A., Beesley N.J., Britton C., Chaudhry U., Doyle S.R., Ezenwa V.O., Fenton A., Howell S.B., Laing R., Mable B.K., Matthews L., McIntyre J., Milne C.E., Morrison T.A., Prentice J.C., Sargison N.D., Williams D.J.L., Wolstenholme A.J., Devaney E.. Refugia and anthelmintic resistance: concepts and challenges.. Int. J. Parasitol. Drugs Drug Resist. 2019;10:51–57.
    pmc: PMC6531808pubmed: 31125837
  10. Kaplan R.M., Nielsen M.K.. An evidence-based approach to equine parasite control: it ain't the 60s anymore.. Equine Vet. Educ. 2010;22:306–316.
  11. 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., Jackson F.. The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants.. Vet. Parasitol. 2009;164:3–11.
    pubmed: 19450930
  12. Klei T.R., Torbert B.J.. Efficacy of ivermectin (22,23-Dihydroavermectin-B1) against gastrointestinal parasites in ponies.. Am. J. Vet. Res. 1980;41:1747–1750.
    pubmed: 6894221
  13. Klei T.R., Rehbein S., Visser M., Langholff W.K., Chapman M.R., French D.D., Hanson P.. Re-evaluation of ivermectin efficacy against equine gastrointestinal parasites.. Vet. Parasitol. 2001;98:315–320.
    pubmed: 11423189
  14. Leathwick D.M.. Modelling the benefits of a new class of anthelmintic in combination.. Vet. Parasitol. 2012;186:93–100.
    pubmed: 22169403
  15. Leathwick D.M., Besier R.B.. The Management of Anthelmintic resistance in grazing ruminants in Australasia – strategies and experiences.. Vet. Parasitol. 2014;204:44–54.
    pubmed: 24439840
  16. Leathwick D.M., Miller C.M., Vlassoff A., Sutherland I.A.. The death rate of Ostertagia circumcincta and Trichostrongylus colubriformis in lactating ewes: implications for anthelmintic resistance.. Int. J. Parasitol. 1997;27:411–416.
    pubmed: 9184933
  17. 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.. Drenching adult ewes: implications of anthelmintic treatments pre- and post-lambing on the development of anthelmintic resistance.. N. Z. Vet. J. 2006;54:297–304.
    pubmed: 17151728
  18. Leathwick D.M., Waghorn T.S., Miller C.M., Candy P.M., Oliver A.-M.B.. Managing anthelmintic resistance — use of a combination anthelmintic and leaving some lambs untreated to slow the development of resistance to ivermectin.. Vet. Parasitol. 2012;187:285–294.
    pubmed: 22244532
  19. Leathwick D.M., Donecker J.M., Nielsen M.K.. A model for the dynamics of the free-living stages of equine cyathostomins.. Vet. Parasitol. 2015;209:210–220.
    pubmed: 25819918
  20. Leathwick D.M., Sauermann C.W., Reinemeyer C.R., Nielsen M.K.. A model for the dynamics of the parasitic stages of equine cyathostomins.. Vet. Parasitol. 2019;268:53–60.
    pubmed: 30981306
  21. Love S., Murphy D., Mellor D.. Pathogenicity of cyathostome infection.. Vet. Parasitol. 1999;85:113–121.
    pubmed: 10485358
  22. Lyons E.T., Drudge J.H., Tolliver S.C.. Antiparasitic activity of ivermectin in critical tests in equids.. Am. J. Vet. Res. 1980;42:2069–2072.
    pubmed: 6452079
  23. Lyons E.T., Tolliver S.C., Collins S.S.. Probable reason why small strongyle EPG counts are returning “early” after ivermectin treatment of horses on a farm in Central Kentucky.. Parasitol. Res. 2009;104:569–574.
    pubmed: 18931857
  24. Lyons E.T., Tolliver S.C., Kuzmina T.A., Collins S.S.. Critical tests evaluating efficacy of moxidectin against small strongyles in horses from a herd for which reduced activity had been found in field tests in Central Kentucky.. Parasitol. Res. 2010;107:1495–1498.
    pubmed: 20714749
  25. Martin P.J., Le Jambre L.F., Claxton J.H.. The impact of refugia on the development of thiabendazole resistance in Haemonchus contortus.. Int. J. Parasitol. 1981;11:35–41.
    pubmed: 7228476
  26. Menne M.J., Williams C.N., Jr., Vose R.S.. United States Historical Climatology Network Daily Temperature, Precipitation, and Snow Data.. .
  27. Nielsen M.K., Branan M.A., Wiedenheft A.M., Digianantonio R., Garber L.P., Kopral C.A., Phillippi-Taylor A.M., Traub-Dargatz J.L.. Parasite control strategies used by equine owners in the United States: a national survey.. Vet. Parasitol. 2018;250:45–51.
    pubmed: 29329623
  28. Nielsen M.K., Sauermann C.W., Leathwick D.M.. The effect of climate, season, and treatment intensity on anthelmintic resistance in cyathostomins: a modelling exercise.. Vet. Parasitol. 2019;269:7–12.
    pubmed: 31079830
  29. Nielsen M.K., Mittel L., Grice A., Erskine M., Graves E., Vaala W., Tully R.C., French D.D., Bowman R., Kaplan R.M.. AAEP Parasite Control Guidelines.. American Association of Equine Practitioners 2019.
  30. Peregrine A.S., Molento M.B., Kaplan R.M., Nielsen M.K.. Anthelmintic resistance in important parasites of horses: does it really matter?. Vet. Parasitol. 2014;201:1–8.
    pubmed: 24485565
  31. Rendle D., Austin C., Bowen M., Cameron I., Furtado T., Hodgkinson J., McGorum B., Matthews J.B.. Equine de-worming: a consensus on current best practice.. UK-Vet Equine 2019;3:1–14.
  32. Robert M., Hu W., Nielsen M.K., Stowe C.J.. Attitudes towards implementation of surveillance-based parasite control on Kentucky Thoroughbred farms – current strategies, awareness, and willingness-to-pay.. Equine Vet. J. 2015;47:694–700.
    pubmed: 25196091
  33. Sauermann C.W., Nielsen M.K., Lou D., Leathwick D.M.. Modelling the development of anthelmintic resistance in cyathostomin parasites: the importance of genetic and fitness parameters.. Vet. Parasitol. 2019;269:28–33.
    pubmed: 31079825
  34. Smith H.J.. Strongyle infections in ponies I. Response to intermittent thiabendazole treatments.. Can. J. Comp. Med. 1976;40:327–333.
    pmc: PMC1277559pubmed: 1000396
  35. Smith H.J.. Experimental Trichonema infections in mature ponies.. Vet. Parasitol. 1978;4:265–273.
  36. Tzelos T., Matthews J.. Anthelmintic Resistance in Equine Helminths and Mitigating its Effects.. In Practice 2016;38:489–499.
  37. Tzelos T., Barbeito J.S., Nielsen M.K., Morgan E.R., Hodgkinson J.E., Matthews J.B.. Strongyle egg reappearance period after moxidectin treatment and its relationship with management factors in UK equine populations.. Vet. Parasitol. 2017;237:70–76.
    pubmed: 28249767
  38. Waghorn T., Leathwick D., Miller C., Atkinson D.. Brave or gullible: testing the concept that leaving susceptible parasites in refugia will slow the development of anthelmintic resistance.. N. Z. Vet. J. 2008;56:158–163.
    pubmed: 18690251
  39. van Wyk J.A.. Refugia—overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance.. Onderstepoort J. Vet. Res. 2001;68:55–67.
    pubmed: 11403431

Citations

This article has been cited 10 times.
  1. Ullah A, Geng M, Chen W, Zhu Q, Shi L, Zhang X, Akhtar MF, Wang C, Khan MZ. Effect of Parasitic Infections on Hematological Profile, Reproductive and Productive Performance in Equines. Animals (Basel) 2025 Nov 14;15(22).
    doi: 10.3390/ani15223294pubmed: 41302002google scholar: lookup
  2. Abbas G, Nielsen MK, E-Hage C, Ghafar A, Beveridge I, Bauquier J, Beasley A, Wilkes EJA, Carrigan P, Cudmore L, Jacobson C, Hughes KJ, Jabbar A. Recent advances in intestinal helminth parasites of horses in the Asia-Pacific region: Current trends, challenges and future directions. Int J Parasitol Drugs Drug Resist 2025 Dec;29:100622.
    doi: 10.1016/j.ijpddr.2025.100622pubmed: 41135277google scholar: lookup
  3. Abbas G, Stevenson MA, Bauquier J, Beasley A, Jacobson C, El-Hage C, Wilkes EJA, Carrigan P, Cudmore L, Hurley J, Beveridge I, Nielsen MK, Hughes KJ, Jabbar A. Assessment of worm control practices recommended by equine veterinarians in Australia. Front Vet Sci 2023;10:1305360.
    doi: 10.3389/fvets.2023.1305360pubmed: 38026649google scholar: lookup
  4. Gómez-Cabrera K, Salas-Romero J, Sifontes JA, de la Torre Cánova R, Salas JE, Nielsen MK. Feasibility of selective anthelmintic therapy to horses in tropical conditions: the Cuban scenario. Trop Anim Health Prod 2021 Nov 15;53(6):545.
    doi: 10.1007/s11250-021-02966-ypubmed: 34779918google scholar: lookup
  5. Diakou A, Prichard RK. Concern for Dirofilaria immitis and Macrocyclic Lactone Loss of Efficacy: Current Situation in the USA and Europe, and Future Scenarios. Pathogens 2021 Oct 14;10(10).
    doi: 10.3390/pathogens10101323pubmed: 34684273google scholar: lookup
  6. Johnson ACB, Biddle AS. The Use of Molecular Profiling to Track Equine Reinfection Rates of Cyathostomin Species Following Anthelmintic Administration. Animals (Basel) 2021 May 9;11(5).
    doi: 10.3390/ani11051345pubmed: 34065099google scholar: lookup
  7. Zanet S, Battisti E, Labate F, Oberto F, Ferroglio E. Reduced Efficacy of Fenbendazole and Pyrantel Pamoate Treatments against Intestinal Nematodes of Stud and Performance Horses. Vet Sci 2021 Mar 5;8(3).
    doi: 10.3390/vetsci8030042pubmed: 33807857google scholar: lookup
  8. Roelfstra L, Quartier M, Pfister K. Preliminary Data from Six Years of Selective Anthelmintic Treatment on Five Horse Farms in France and Switzerland. Animals (Basel) 2020 Dec 15;10(12).
    doi: 10.3390/ani10122395pubmed: 33333748google scholar: lookup
  9. Sauermann CW, Leathwick DM, Lieffering M, Nielsen MK. Climate change is likely to increase the development rate of anthelmintic resistance in equine cyathostomins in New Zealand. Int J Parasitol Drugs Drug Resist 2020 Dec;14:73-79.
    doi: 10.1016/j.ijpddr.2020.09.001pubmed: 32992276google scholar: lookup
  10. Rose Vineer H. What Modeling Parasites, Transmission, and Resistance Can Teach Us. Vet Clin North Am Food Anim Pract 2020 Mar;36(1):145-158.
    doi: 10.1016/j.cvfa.2019.11.002pubmed: 32029180google scholar: lookup