Anthelmintic resistance in nematodes of horses.
Abstract: Suppressive anthelmintic treatment strategies originally designed to control Strongylus vulgaris in horses were extremely successful in reducing morbidity and mortality from parasitic disease. Unfortunately, this strategy has inadvertently resulted in the selection of drug-resistant cyathostomes (Cyathostominea), which are now considered the principal parasitic pathogens of horses. Resistance in the cyathostomes to benzimidazole drugs is highly prevalent throughout the world, and resistance to pyrantel appears to be increasingly common. However, there are still no reports of ivermectin resistance in nematode parasites of horses despite 20 years of use. It is unknown why resistance to ivermectin has not yet emerged, but considering that ivermectin is the single most commonly used anthelmintic in horses most parasitologists agree that resistance is inevitable. The fecal egg count reduction test is considered the gold standard for clinical diagnosis of anthelmintic resistance in horses, but diagnosis is complicated by lack of an accepted standard for the performance of this test or for the analysis and interpretation of data. Presently there is very little data available on the molecular mechanisms of anthelmintic resistance in cyathostomes; beta-tubulin gene is the only anthelmintic-resistance associated gene that has been cloned. The increasingly high prevalence of anthelmintic-resistant cyathostomes must be taken into account when designing worm control programs for horses. Strategies to decelerate further selection for drug resistance thereby extending the lifetime of currently effective anthelmintics should be implemented whenever possible. Considering the nature of the equine industry in which horses often graze shared pastures with horses from diverse locations, transmission and widespread dispersal of resistant parasites is virtually assured. A proactive approach to this problem centered on understanding the molecular basis of anthelmintic resistance in cyathostomes is required if we are to expect chemical control of nematodes in horses to remain a viable element of parasite control in the future.
Publication Date: 2002-10-22 PubMed ID: 12387486DOI: 10.1051/vetres:2002035Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Review
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.
The article’s focus is on the growing issue of drug-resistant parasites in horses, specifically nematodes known as cyathostomes. The research explores various aspects such as the prevalence, detection, molecular mechanisms involved in this resistance and proposes strategies for managing this resistance in future.
Background
- The report begins by discussing the success of initially designed suppressive anthelmintic treatment strategies in controlling a type of parasite in horses called Strongylus vulgaris, which resulted in a significant reduction in disease-related morbidity and mortality.
- Despite this success, the strategy has unintentionally contributed to the selection and emergence of drug-resistant cyathostomes, which pose a significant health risk to horses due to their resistance to commonly used drugs like benzimidazole.
Anthelmintic Resistance
- The report cites drug resistance in cyathostomes as a global problem. Resistance to benzimidazole drugs is widespread, while resistance to another anthelmintic drug, pyrantel, is reportedly on the rise.
- However, there are no reported cases of resistance to ivermectin, another common antiparasitic medicine, even after two decades of its use. The reason for this remains unclear, although the authors predict it’s inevitable given its extensive usage.
Diagnosis of Anthelmintic Resistance
- The fecal egg count reduction test is considered the gold standard technique for diagnosing anthelmintic resistance. However, its complexity and lack of universally accepted standards for execution, analysis, and interpretation pose significant challenges.
Molecular Basis of Anthelmintic Resistance
- Currently, there’s minimal data available on the molecular mechanisms underlying drug resistance in cyathostomes.
- The beta-tubulin gene is the only known gene linked with resistance against anthelmintics. Understanding these molecular mechanisms can help develop effective strategies to combat drug resistance.
Future Strategies
- Considering the increasing prevalence of anthelmintic-resistant cyathostomes, it’s crucial to incorporate this factor when designing future parasite control programs.
- Strategies to slow down further drug resistance selection, thus extending the lifetime of currently effective drugs, are deemed necessary.
- A proactive approach to this problem involves understanding the molecular basis of anthelmintic resistance in cyathostomes, which is seen as crucial in maintaining chemical control of nematodes as a viable option for parasite control in horses.
Cite This Article
APA
Kaplan RM.
(2002).
Anthelmintic resistance in nematodes of horses.
Vet Res, 33(5), 491-507.
https://doi.org/10.1051/vetres:2002035 Publication
Researcher Affiliations
- Department of Medical Microbiology and Parasitology, College of Veterinary Medicine, University of Georgia, Athens 30602, USA. rkaplan@vet.uga.edu
MeSH Terms
- Animals
- Anthelmintics / pharmacology
- Anthelmintics / therapeutic use
- Benzimidazoles / pharmacology
- Benzimidazoles / therapeutic use
- Drug Resistance
- Feces / parasitology
- Horse Diseases / drug therapy
- Horse Diseases / parasitology
- Horse Diseases / prevention & control
- Horses
- Ivermectin / pharmacology
- Ivermectin / therapeutic use
- Nematoda / drug effects
- Nematode Infections / drug therapy
- Nematode Infections / prevention & control
- Nematode Infections / veterinary
- Parasite Egg Count / veterinary
- Pyrantel / pharmacology
- Pyrantel / therapeutic use
- Strongyloidea / drug effects
- Treatment Outcome
References
This article includes 106 references
Citations
This article has been cited 57 times.- Carbonell JD, Fernández N, Escobar MJ, Álvarez MT, Sánchez L, Hernández A, Meana A. Comparative Efficacy of Topical Pyrethroids and Benzoyl Peroxide for Treating Chorioptic Mange in Spanish-Breton Horses. J Parasitol Res 2025;2025:8948099.
- Merridale-Punter MS, Wiethoelter AK, El-Hage CM, Patrick C, Hitchens PL. Common clinical findings identified in working equids in low- and middle-income countries from 2005 to 2021. PLoS One 2024;19(6):e0304755.
- Shaver AO, Miller IR, Schaye ES, Moya ND, Collins JB, Wit J, Blanco AH, Shao FM, Andersen EJ, Khan SA, Paredes G, Andersen EC. Quantifying the fitness effects of resistance alleles with and without anthelmintic selection pressure using Caenorhabditis elegans. PLoS Pathog 2024 May;20(5):e1012245.
- Mostafa NA, Hamdi SAH, Fol MF. Potential anthelmintic effect of chitosan on Syphacia muris infecting Wistar rats: biochemical, immunological, and histopathological studies. Sci Rep 2024 Feb 3;14(1):2825.
- Boelow H, Krücken J, von Samson-Himmelstjerna G. Epidemiological study on factors influencing the occurrence of helminth eggs in horses in Germany based on sent-in diagnostic samples. Parasitol Res 2023 Mar;122(3):749-767.
- Nielsen MK. Anthelmintic resistance in equine nematodes: Current status and emerging trends. Int J Parasitol Drugs Drug Resist 2022 Dec;20:76-88.
- Dauparaitė E, Kupčinskas T, Varady M, Petkevičius S. Anthelmintic resistance of horse strongyle nematodes to fenbendazole in Lithuania. Acta Vet Scand 2022 Sep 15;64(1):26.
- Malsa J, Courtot É, Boisseau M, Dumont B, Gombault P, Kuzmina TA, Basiaga M, Lluch J, Annonay G, Dhorne-Pollet S, Mach N, Sutra JF, Wimel L, Dubois C, Guégnard F, Serreau D, Lespine A, Sallé G, Fleurance G. Effect of sainfoin (Onobrychis viciifolia) on cyathostomin eggs excretion, larval development, larval community structure and efficacy of ivermectin treatment in horses. Parasitology 2022 Sep;149(11):1439-1449.
- Jürgenschellert L, Krücken J, Bousquet E, Bartz J, Heyer N, Nielsen MK, von Samson-Himmelstjerna G. Occurrence of Strongylid Nematode Parasites on Horse Farms in Berlin and Brandenburg, Germany, With High Seroprevalence of Strongylus vulgaris Infection. Front Vet Sci 2022;9:892920.
- Boelow H, Krücken J, Thomas E, Mirams G, von Samson-Himmelstjerna G. Comparison of FECPAK(G2), a modified Mini-FLOTAC technique and combined sedimentation and flotation for the coproscopic examination of helminth eggs in horses. Parasit Vectors 2022 May 12;15(1):166.
- Elmeligy E, Abdelbaset A, Elsayed HK, Bayomi SA, Hafez A, Abu-Seida AM, El-Khabaz KAS, Hassan D, Ghandour RA, Khalphallah A. Oxidative stress in Strongylus spp. infected donkeys treated with piperazine citrate versus doramectin. Open Vet J 2021 Apr-Jun;11(2):238-250.
- 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).
- Dauparaitė E, Kupčinskas T, von Samson-Himmelstjerna G, Petkevičius S. Anthelmintic resistance of horse strongyle nematodes to ivermectin and pyrantel in Lithuania. Acta Vet Scand 2021 Jan 25;63(1):5.
- Nielsen MK, Banahan M, Kaplan RM. Importation of macrocyclic lactone resistant cyathostomins on a US thoroughbred farm. Int J Parasitol Drugs Drug Resist 2020 Dec;14:99-104.
- Hedberg-Alm Y, Penell J, Riihimäki M, Osterman-Lind E, Nielsen MK, Tydén E. Parasite Occurrence and Parasite Management in Swedish Horses Presenting with Gastrointestinal Disease-A Case-Control Study. Animals (Basel) 2020 Apr 7;10(4).
- Fairweather I, Brennan GP, Hanna REB, Robinson MW, Skuce PJ. Drug resistance in liver flukes. Int J Parasitol Drugs Drug Resist 2020 Apr;12:39-59.
- Tang L, Xiu Y, Yan L, Cui Y, Ma X, Ente M, Zhang Y, Li K, Zhang D. Drug Efficacy of Ivermectin Against Primary Nematodes Parasitizing Captive Przewalski's Horse (Equus Ferus Przewalskii) after Ten Years of Annually Treatment. Helminthologia 2020 Mar;57(1):57-62.
- Tinkler SH. Preventive chemotherapy and anthelmintic resistance of soil-transmitted helminths - Can we learn nothing from veterinary medicine?. One Health 2020 Jun;9:100106.
- Harvey AM, Meggiolaro MN, Hall E, Watts ET, Ramp D, Šlapeta J. Wild horse populations in south-east Australia have a high prevalence of Strongylus vulgaris and may act as a reservoir of infection for domestic horses. Int J Parasitol Parasites Wildl 2019 Apr;8:156-163.
- Charvet CL, Guégnard F, Courtot E, Cortet J, Neveu C. Nicotine-sensitive acetylcholine receptors are relevant pharmacological targets for the control of multidrug resistant parasitic nematodes. Int J Parasitol Drugs Drug Resist 2018 Dec;8(3):540-549.
- Misuno E, Clark CR, Anderson SL, Jenkins E, Wagner B, Dembek K, Petrie L. Characteristics of parasitic egg shedding over a 1-year period in foals and their dams in 2 farms in central Saskatchewan. Can Vet J 2018 Mar;59(3):284-292.
- Pyziel AM, Björck S, Wiklund R, Skarin M, Demiaszkiewicz AW, Höglund J. Gastrointestinal parasites of captive European bison Bison bonasus (L.) with a sign of reduced efficacy of Haemonchus contortus to fenbendazole. Parasitol Res 2018 Jan;117(1):295-302.
- Bredtmann CM, Krücken J, Murugaiyan J, Kuzmina T, von Samson-Himmelstjerna G. Nematode Species Identification-Current Status, Challenges and Future Perspectives for Cyathostomins. Front Cell Infect Microbiol 2017;7:283.
- Zak A, Siwinska N, Slowikowska M, Borowicz H, Kubiak K, Hildebrand J, Popiolek M, Niedzwiedz A. Searching for ivermectin resistance in a Strongylidae population of horses stabled in Poland. BMC Vet Res 2017 Jul 3;13(1):210.
- Kaspar A, Pfister K, Nielsen MK, Silaghi C, Fink H, Scheuerle MC. Detection of Strongylus vulgaris in equine faecal samples by real-time PCR and larval culture - method comparison and occurrence assessment. BMC Vet Res 2017 Jan 11;13(1):19.
- Fischer JK, Hinney B, Denwood MJ, Traversa D, von Samson-Himmelstjerna G, Clausen PH. Efficacy of selected anthelmintic drugs against cyathostomins in horses in the federal state of Brandenburg, Germany. Parasitol Res 2015 Dec;114(12):4441-50.
- Borji H, Moosavi Z, Ahmadi F. Cranial Mesenteric Arterial Obstruction Due To Strongylus vulgaris Larvae in a Donkey (Equus asinus). Iran J Parasitol 2014 Sep;9(3):441-4.
- Lott MJ, Hose GC, Isberg SR, Power ML. Genetics and infection dynamics of Paratrichosoma sp in farmed saltwater crocodiles (Crocodylus porosus). Parasitol Res 2015 Feb;114(2):727-35.
- Schneider S, Pfister K, Becher AM, Scheuerle MC. Strongyle infections and parasitic control strategies in German horses - a risk assessment. BMC Vet Res 2014 Nov 12;10:262.
- Pulaski CN, Malone JB, Bourguinat C, Prichard R, Geary T, Ward D, Klei TR, Guidry T, Smith G', Delcambre B, Bova J, Pepping J, Carmichael J, Schenker R, Pariaut R. Establishment of macrocyclic lactone resistant Dirofilaria immitis isolates in experimentally infected laboratory dogs. Parasit Vectors 2014 Nov 7;7:494.
- Corbett CJ, Love S, Moore A, Burden FA, Matthews JB, Denwood MJ. The effectiveness of faecal removal methods of pasture management to control the cyathostomin burden of donkeys. Parasit Vectors 2014 Jan 24;7:48.
- Scantlebury CE, Peachey L, Hodgkinson J, Matthews JB, Trawford A, Mulugeta G, Tefera G, Pinchbeck GL. Participatory study of medicinal plants used in the control of gastrointestinal parasites in donkeys in Eastern Shewa and Arsi zones of Oromia region, Ethiopia. BMC Vet Res 2013 Sep 11;9:179.
- Lyons ET, Tolliver SC, Kuzmina TA. Investigation of strongyle EPG values in horse mares relative to known age, number positive, and level of egg shedding in field studies on 26 farms in Central Kentucky (2010-2011). Parasitol Res 2012 Jun;110(6):2237-45.
- Kuzmina TA. Contamination of the environment by strongylid (Nematoda: Strongylidae) infective larvae at horse farms of various types in Ukraine. Parasitol Res 2012 May;110(5):1665-74.
- Lyons ET, Kuzmina TA, Tolliver SC, Collins SS. Observations on development of natural infection and species composition of small strongyles in young equids in Kentucky. Parasitol Res 2011 Dec;109(6):1529-35.
- Hinney B, Wirtherle NC, Kyule M, Miethe N, Zessin KH, Clausen PH. A questionnaire survey on helminth control on horse farms in Brandenburg, Germany and the assessment of risks caused by different kinds of management. Parasitol Res 2011 Dec;109(6):1625-35.
- Blackhall WJ, Kuzmina T, von Samson-Himmelstjerna G. β-Tubulin genotypes in six species of cyathostomins from anthelmintic-naive Przewalski and benzimidazole-resistant brood horses in Ukraine. Parasitol Res 2011 Oct;109(4):1199-203.
- Buxton SK, Neveu C, Charvet CL, Robertson AP, Martin RJ. On the mode of action of emodepside: slow effects on membrane potential and voltage-activated currents in Ascaris suum. Br J Pharmacol 2011 Sep;164(2b):453-70.
- Becher AM, Pfister K. [The efficacy of anthelmintic drugs against horse strongyles in the area of Salzburg and preliminary results of selective anthelmintic treatment]. Wien Klin Wochenschr 2010 Oct;122 Suppl 3:71-5.
- Cantacessi C, Mitreva M, Campbell BE, Hall RS, Young ND, Jex AR, Ranganathan S, Gasser RB. First transcriptomic analysis of the economically important parasitic nematode, Trichostrongylus colubriformis, using a next-generation sequencing approach. Infect Genet Evol 2010 Dec;10(8):1199-207.
- Araujo JM, Araújo JV, Braga FR, Carvalho RO. In vitro predatory activity of nematophagous fungi and after passing through gastrointestinal tract of equine on infective larvae of Strongyloides westeri. Parasitol Res 2010 Jun;107(1):103-8.
- Nielsen MK. Restrictions of anthelmintic usage: perspectives and potential consequences. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S7.
- Lake SL, Matthews JB, Kaplan RM, Hodgkinson JE. Determination of genomic DNA sequences for beta-tubulin isotype 1 from multiple species of cyathostomin and detection of resistance alleles in third-stage larvae from horses with naturally acquired infections. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S6.
- von Samson-Himmelstjerna G, Traversa D, Demeler J, Rohn K, Milillo P, Schurmann S, Lia R, Perrucci S, di Regalbono AF, Beraldo P, Barnes H, Cobb R, Boeckh A. Effects of worm control practices examined by a combined faecal egg count and questionnaire survey on horse farms in Germany, Italy and the UK. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S3.
- Traversa D, von Samson-Himmelstjerna G, Demeler J, Milillo P, Schürmann S, Barnes H, Otranto D, Perrucci S, di Regalbono AF, Beraldo P, Boeckh A, Cobb R. Anthelmintic resistance in cyathostomin populations from horse yards in Italy, United Kingdom and Germany. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S2.
- Corning S. Equine cyathostomins: a review of biology, clinical significance and therapy. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S1.
- Traversa D, Otranto D. Biotechnological advances in the diagnosis of little-known parasitoses of pets. Parasitol Res 2009 Jan;104(2):209-16.
- Lia RP, Traversa D, Iorio R, Otranto D, Klei TR, Ricci V, Giangaspero A. Preliminary molecular identification of drug resistant cyathostomes in Italy. Vet Res Commun 2008 Sep;32 Suppl 1:S211-3.
- Slocombe JO, Coté JF, de Gannes RV. The persistence of benzimidazole-resistant cyathostomes on horse farms in Ontario over 10 years and the effectiveness of ivermectin and moxidectin against these resistant strains. Can Vet J 2008 Jan;49(1):56-60.
- Lind EO, Rautalinko E, Uggla A, Waller PJ, Morrison DA, Höglund J. Parasite control practices on Swedish horse farms. Acta Vet Scand 2007 Sep 26;49(1):25.
- Traversa D, Iorio R, Klei TR, Kharchenko VA, Gawor J, Otranto D, Sparagano OA. New method for simultaneous species-specific identification of equine strongyles (nematoda, strongylida) by reverse line blot hybridization. J Clin Microbiol 2007 Sep;45(9):2937-42.
- Lind EO, Kuzmina T, Uggla A, Waller PJ, Höglund J. A field study on the effect of some anthelmintics on cyathostomins of horses in sweden. Vet Res Commun 2007 Jan;31(1):53-65.
- Blackhall WJ, Drogemuller M, Schnieder T, von Samson-Himmelstjerna G. Expression of recombinant beta-tubulin alleles from Cylicocyclus nassatus (Cyathostominae). Parasitol Res 2006 Nov;99(6):687-93.
- Lyons ET, Tolliver SC, Collins SS. Field studies on endoparasites of Thoroughbred foals on seven farms in central Kentucky in 2004. Parasitol Res 2006 Apr;98(5):496-500.
- Hodgkinson JE, Freeman KL, Lichtenfels JR, Palfreman S, Love S, Matthews JB. Identification of strongyle eggs from anthelmintic-treated horses using a PCR-ELISA based on intergenic DNA sequences. Parasitol Res 2005 Mar;95(4):287-92.
- Cirak VY, Güleğen E, Bauer C. Benzimidazole resistance in cyathostomin populations on horse farms in western Anatolia, Turkey. Parasitol Res 2004 Aug;93(5):392-5.
- Lyons ET, Tolliver SC. Prevalence of parasite eggs (Strongyloides westeri, Parascaris equorum, and strongyles) and oocysts (Emeria leuckarti) in the feces of Thoroughbred foals on 14 farms in central Kentucky in 2003. Parasitol Res 2004 Mar;92(5):400-4.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists