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International journal for parasitology. Drugs and drug resistance2023; 24; 100517; doi: 10.1016/j.ijpddr.2023.11.006

A national survey of anthelmintic resistance in ascarid and strongylid nematodes in Australian Thoroughbred horses.

Abstract: This study quantified the extent of anthelmintic resistance (AR) in ascarid and strongylid nematodes against commonly used anthelmintics in Australian Thoroughbred horses. Faecal egg count reduction tests (FECRTs, n = 86) and egg reappearance period (ERP) tests were conducted on 22 farms across Australia. Faecal egg counts (FECs) were determined using the modified McMaster technique, and percent faecal egg count reduction (%FECR) was calculated using the Bayesian hierarchical model and hybrid Frequentist/Bayesian analysis method. The results were interpreted using old (published in 1992) and new (2023) research guidelines of the World Association for the Advancement of Veterinary Parasitology (WAAVP). The species composition of strongylid nematodes was detected utilising a DNA-metabarcoding method using pre- and post-treatment samples. Resistance was observed in strongylid nematodes to commonly used single-active and combination anthelmintics, including ivermectin (IVM %FECR range: 82%-92%; 95% lower credible interval (LCI) range: 80%-90%), abamectin (ABM: 73%-92%; 65%-88%), moxidectin (MOX: 89%-91%; 84%-89%), oxfendazole (OFZ: 0%-56%; 0%-31%) and its combination with pyrantel (OFZ + PYR: 0%-82%; 0%-78%). Resistance in Parascaris spp. was observed to IVM (10%-43%; 0%-36%), ABM (0%; 0%) and MOX (0%; 0%). When the new thresholds recommended by the WAAVP were used, AR was detected in six additional FECRTs for strongylids and three more tests for Parascaris spp., introducing resistance to OFZ and OFZ + PYR in the latter. Shortened ERPs (4-6 weeks) of strongylids were observed in 31 FECRTs in which AR was not detected at 2 weeks post-treatment for all the anthelmintics tested. Among cyathostomins, Cylicocyclus nassatus, Cylicostephanus longibursatus and Coronocyclus coronatus were the most prevalent species at 2 weeks post-treatment, whereas the main species appearing at five weeks following treatments with macrocyclic lactones were Cylicocyclus nassatus, Cylicostephanus longibursatus and Cylicocyclus ashworthi. After treatment with OFZ + PYR, the latter three, plus Coronocyclus coronatus and Cyathostomum catinatum, were detected at 5 weeks post-treatment. Overall, the study highlights the prevalence of AR in both ascarids and strongylid nematodes against commonly used anthelmintic products to control worms in Australian horses. The results indicate that ML combination products provided acceptable efficacy at 2 weeks. However, ERP calculations suggest that products work less effectively than previously measured. It is suggested to regularly monitor the efficacy of the anthelmintics and consider changing the worm control practices to better manage worms and AR in Australian horses.
Copyright © 2023 The Authors. Published by Elsevier Ltd.. All rights reserved.
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Publication Date: 2023-11-29 PubMed ID: 38064906PubMed Central: PMC10757041DOI: 10.1016/j.ijpddr.2023.11.006Google Scholar: Lookup
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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 research article discusses a study carried out to measure the resistance against certain kinds of deworming drugs (anthelmintics) in two types of parasitic worms (ascarid and strongylid nematodes) found in thoroughbred horses in Australia.

Overview of Study and Methodology

  • The study sought to provide insights into the extent of anthelmintic resistance (AR) in ascarid and strongylid nematodes, particularly against popular anthelmintics used in Australian Thoroughbred horses.
  • Across 22 farms in Australia, Faecal egg count reduction tests (FECRTs, n = 86) and egg reappearance period (ERP) tests were conducted to understand the effects of these drugs on the worms.
  • Techniques like the modified McMaster technique were used to determine Faecal egg counts (FEC) while %FECR (percent faecal egg count reduction) was computed using the Bayesian hierarchical model and hybrid Frequentist/Bayesian analysis method.
  • Results were then interpreted using both old (1992) and new (2023) guidelines issued by the World Association for the Advancement of Veterinary Parasitology (WAAVP).
  • A DNA-metabarcoding method was used in determining the species composition of strongylid nematodes, using pre- and post-treatment samples.

Results and Analysis

  • Resistance was seen in strongylid nematodes against commonly used single-active and combination anthelmintics such as ivermectin, abamectin, moxidectin, oxfendazole, and its combination with pyrantel.
  • Resistance in Parascaris spp. worm species was observed to ivermectin, abamectin and moxidectin.
  • Using the newer thresholds recommended by the WAAVP led to AR being detected in more tests, implying that the resistance was more prevalent than previously thought.
  • Observations were also made on the decreased time (4-6 weeks) taken for eggs to reappear in tests where AR wasn’t detected at the fortnightly post-treatment mark. This suggests a potential speedier reproduction which could be due to AR.
  • Post-treatment, the more common worm species were Cylicocyclus nassatus, Cylicostephanus longibursatus, and Coronocyclus coronatus. Certain species had more prominent occurrences depending on the specific treatment administered.

Conclusions and Recommendations

  • The study brings to light the widespread issue of AR in ascarids and strongylid nematodes against familiar anthelmintic products used against horse worms in Australia.
  • While macrocyclic lactone combination products indicate satisfactory efficiency at two weeks, ERPs suggest that they might work less effectively than previously understood.
  • The paper concludes with a suggestion urging regular monitoring of anthelmintics’ effectiveness and reconsideration of worm control practices for better management of AR in Australian Equines.

Cite This Article

APA
Abbas G, Ghafar A, McConnell E, Beasley A, Bauquier J, Wilkes EJA, El-Hage C, Carrigan P, Cudmore L, Hurley J, Gauci CG, Beveridge I, Ling E, Jacobson C, Stevenson MA, Nielsen MK, Hughes KJ, Jabbar A. (2023). A national survey of anthelmintic resistance in ascarid and strongylid nematodes in Australian Thoroughbred horses. Int J Parasitol Drugs Drug Resist, 24, 100517. https://doi.org/10.1016/j.ijpddr.2023.11.006

Publication

International journal for parasitology. Drugs and drug resistance
ISSN: 2211-3207
NlmUniqueID: 101576715
Country: Netherlands
Language: English
Volume: 24
Pages: 100517

Researcher Affiliations

Abbas, Ghazanfar
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
Ghafar, Abdul
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
McConnell, Emma
  • Centre for Animal Production and Health, Murdoch University, Murdoch, Western Australia, Australia.
Beasley, Anne
  • School of Agriculture and Food Sustainability, University of Queensland, Gatton, Queensland 4343, Australia.
Bauquier, Jenni
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
Wilkes, Edwina J A
  • Racing Victoria, Flemington, Victoria 3031, Australia.
El-Hage, Charles
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
Carrigan, Peter
  • Scone Equine Hospital, Scone, New South Wales 2337, Australia.
Cudmore, Lucy
  • Scone Equine Hospital, Scone, New South Wales 2337, Australia.
Hurley, John
  • Swettenham Stud, Nagambie, Victoria 3608, Australia.
Gauci, Charles G
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
Beveridge, Ian
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
Ling, Elysia
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
Jacobson, Caroline
  • Centre for Animal Production and Health, Murdoch University, Murdoch, Western Australia, Australia.
Stevenson, Mark A
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia.
Nielsen, Martin K
  • M.H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, KY, USA.
Hughes, Kristopher J
  • School of Agricultural, Environmental and Veterinary Sciences, Charles Sturt University, Wagga Wagga, New South Wales 2650, Australia.
Jabbar, Abdul
  • Melbourne Veterinary School, The University of Melbourne, Werribee, Victoria 3030, Australia. Electronic address: jabbara@unimelb.edu.au.

MeSH Terms

  • Animals
  • Anthelmintics / pharmacology
  • Australia / epidemiology
  • Bayes Theorem
  • Drug Resistance
  • Feces / parasitology
  • Horse Diseases / drug therapy
  • Horse Diseases / parasitology
  • Horses
  • Parasite Egg Count / veterinary
  • Strongyloidea / genetics

Conflict of Interest Statement

Declaration of competing interest The authors of this manuscript are members of the Australian Equine Parasitology Advisory Panel (AEPAP), including Abdul Jabbar, Ghazanfar Abbas, Jenni Bauquier, Charles El-Hage, Abdul Ghafar and Ian Beveridge (The University of Melbourne), Anne Beasley (University of Queensland), Kristopher Hughes (Charles Sturt University), Caroline Jacobson and Emma McConnell (Murdoch University), Edwina Wilkes (Racing Victoria), Peter Carrigan and Lucy Cudmore (Scone Equine Hospital) and John Hurley (Swettenham Stud). Boehringer Ingelheim supported the panel. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

This article includes 97 references
  1. Abbas G, Ghafar A, Hurley J, Bauquier J, Beasley A, Wilkes EJA, Jacobson C, El-Hage C, Cudmore L, Carrigan P, Tennent-Brown B, Gauci CG, Nielsen MK, Hughes KJ, Beveridge I, Jabbar A. Cyathostomin resistance to moxidectin and combinations of anthelmintics in Australian horses.. Parasites Vectors 2021;14:597.
    pmc: PMC8645149pubmed: 34863271
  2. 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.
    pmc: PMC10654783pubmed: 38026649
  3. Abbas G, Ghafar A, Bauquier J, Beasley A, Ling E, Gauci CG, El-Hage C, Wilkes EJA, McConnell E, Carrigan P, Cudmore L, Hurley J, Beveridge I, Nielsen MK, Stevenson MA, Jacobson C, Hughes KJ, Jabbar A. Prevalence and diversity of ascarid and strongylid nematodes in Australian Thoroughbred horses using next-generation sequencing and bioinformatics tools.. Vet Parasitol 2023;323.
    pubmed: 37844388
  4. Armstrong SK, Woodgate RG, Gough S, Heller J, Sangster NC, Hughes KJ. The efficacy of ivermectin, pyrantel and fenbendazole against Parascaris equorum infection in foals on farms in Australia.. Vet Parasitol 2014;205:575–580.
    pubmed: 25224788
  5. Bartram DJ, Leathwick DM, Taylor MA, Geurden T, Maeder SJ. The role of combination anthelmintic formulations in the sustainable control of sheep nematodes.. Vet Parasitol 2012;186:151–158.
    pubmed: 22245073
  6. Beasley AM, Kotze AC, Allen K, Coleman GT. A survey of macrocyclic lactone efficacy in Australian cyathostomin populations.. Vet Parasitol Reg Stud Rep 2017;8:127–132.
    pubmed: 31014629
  7. Beasley AM, Kotze AC, Barnes TS, Coleman GT. Equine helminth prevalence and management practices on Australian properties as shown by coprological survey and written questionnaire.. Anim Prod Sci 2020;60:2131–2144.
  8. Bellaw JL, Nielsen MK. Meta-analysis of cyathostomin species-specific prevalence and relative abundance in domestic horses from 1975-2020: emphasis on geographical region and specimen collection method.. Parasites Vectors 2020;13:509.
    pmc: PMC7552500pubmed: 33046130
  9. Bellaw JL, Krebs K, Reinemeyer CR, Norris JK, Scare JA, Pagano S, Nielsen MK. Anthelmintic therapy of equine cyathostomin nematodes - larvicidal efficacy, egg reappearance period, and drug resistance.. Int J Parasitol 2018;48:97–105.
    pubmed: 29050919
  10. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.. Nat Biotechnol 2019;37:852–857.
    pmc: PMC7015180pubmed: 31341288
  11. Bull KE, Allen KJ, Hodgkinson JE, Peachey LE. The first report of macrocyclic lactone resistant cyathostomins in the UK.. Int J Parasitol Drugs Drug Resist 2023;21:125–130.
    pmc: PMC10036890pubmed: 36940551
  12. Butler AJ, Greenbank H, Parrish R, Nielsen MK, Stoughton WB. Prevalence of anthelmintic resistant cyathostomins in prince Edward Island, Canada.. Vet Parasitol Reg Stud Rep 2021;26.
    pubmed: 34879940
  13. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data.. Nat Methods 2016;13:581–583.
    pmc: PMC4927377pubmed: 27214047
  14. Callahan BJ, McMurdie PJ, Holmes SP. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis.. ISME J 2017;11:2639–2643.
    pmc: PMC5702726pubmed: 28731476
  15. Canever RJ, Braga PR, Boeckh A, Grycajuck M, Bier D, Molento MB. Lack of Cyathostomin sp. reduction after anthelmintic treatment in horses in Brazil.. Vet Parasitol 2013;194:35–39.
    pubmed: 23318166
  16. Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA, Waller PJ. 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.. Vet Parasitol 1992;44:35–44.
    pubmed: 1441190
  17. Courtot É, Boisseau M, Dhorne-Pollet S, Serreau D, Gesbert A, Reigner F, Basiaga M, Kuzmina T, Lluch J, Annonay G, Kuchly C, Diekmann I, Krücken J, von Samson-Himmelstjerna G, Mach N, Sallé G. Comparison of two molecular barcodes for the study of equine strongylid communities with amplicon sequencing.. PeerJ 2023;11.
    pmc: PMC10105562pubmed: 37070089
  18. Cribb N, Cote N, Boure L, Peregrine A. Acute small intestinal obstruction associated with Parascaris equorum infection in young horses: 25 cases (1985–2004). N Z Vet J 2006;54:338–343.
    pubmed: 17151735
  19. Denwood MJ, Kaplan RM, McKendrick IJ, Thamsborg SM, Nielsen MK, Levecke B. A statistical framework for calculating prospective sample sizes and classifying efficacy results for faecal egg count reduction tests in ruminants, horses and swine.. Vet Parasitol 2023;314.
    pubmed: 36621042
  20. Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data.. Nucleic Acids Res 2017;45:W180–W188.
    pmc: PMC5570177pubmed: 28449106
  21. Edward CL, Hoffmann AA. Ivermectin resistance in a horse in Australia.. Vet Rec 2008;162:56.
    pubmed: 18192659
  22. Flores AG, Osmari V, Ramos Fernanda, Marques C, Jaques Ramos D, Botton S, Flores Vogel F, Antônio Sangioni L. Multiple resistance in equine cyathostomins: a case study from military establishments in Rio Grande do Sul, Brazil.. Rev Bras Parasitol Vet 2020;28(3):29.
    pubmed: 33027421
  23. Gasser RB, Chilton NB, Hoste H, Beveridge I. Rapid sequencing of rDNA from single worms and eggs of parasitic helminths.. Nucleic Acids Res 1993;21:2525–2526.
    pmc: PMC309567pubmed: 8506152
  24. Geary TG, Hosking BC, Skuce PJ, von Samson-Himmelstjerna G, Maeder S, Holdsworth P, Pomroy W, Vercruysse J. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) Guideline: anthelmintic combination products targeting nematode infections of ruminants and horses.. Vet Parasitol 2012;190:306–316.
  25. Geurden T, van Doorn D, Claerebout E, Kooyman F, De Keersmaecker S, Vercruysse J, Besognet B, Vanimisetti B, di Regalbono AF, 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
  26. Ghafar A, Abbas G, King J, Jacobson C, Hughes KJ, El-Hage C, Beasley A, Bauquier J, Wilkes EJA, Hurley J, Cudmore L, Carrigan P, Tennent-Brown B, Nielsen MK, Gauci CG, Beveridge I, Jabbar A. Comparative studies on faecal egg counting techniques used for the detection of gastrointestinal parasites of equines: a systematic review.. Curr Res Parasitol Vector Borne Dis 2021;1.
    pmc: PMC8906068pubmed: 35284858
  27. Ghafar A, Abbas G, Beasley A, Bauquier J, Wilkes EJA, Jacobson C, McConnell E, El-Hage C, Carrigan P, Cudmore L, Tennent-Brown B, Hurley J, Nielsen MK, Gauci CG, Beveridge I, Hughes KJ, Jabbar A. Molecular diagnostics for gastrointestinal helminths in equids: past, present and future.. Vet Parasitol 2023;313.
    pubmed: 36521296
  28. Gordon HM, Whitlock HV. A new technique for counting nematode eggs in sheep faeces.. J Sci Ind Res 1939;12:50–52.
  29. Hutchinson GW, Abba SA, Mfitilodze MW. Seasonal translation of equine strongyle infective larvae to herbage in tropical Australia.. Vet Parasitol 1989;33:251–263.
    pubmed: 2815535
  30. Johnson ACB, Biddle AS. The use of molecular profiling to track equine reinfection rates of cyathostomin species following anthelmintic administration.. Animals 2021;11:1345.
    pmc: PMC8150961pubmed: 34065099
  31. Kaplan RM, Nielsen MK. An evidence-based approach to equine parasite control: it ain't the 60s anymore.. Equine Vet Educ 2010;22:306–316.
  32. Kaplan R, West EM, Norat‐Collazo LM, Vargas J. A combination treatment strategy using pyrantel pamoate and oxibendazole demonstrates additive effects for controlling equine cyathostomins.. Equine Vet Educ 2014;26:485–491.
  33. Kaplan RM, Denwood MJ, Nielsen MK, Thamsborg SM, Torgerson PR, Gilleard JS, Dobson RJ, Vercruysse J, Levecke B. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) guideline for diagnosing anthelmintic resistance using the faecal egg count reduction test in ruminants, horses and swine.. Vet Parasitol 2023;318.
    pubmed: 37121092
  34. Kooyman F, Van Doorn D, Geurden T, Mughini-Gras L, Ploeger HW, Wagenaar J. Species composition of larvae cultured after anthelmintic treatment indicates reduced moxidectin susceptibility of immature Cylicocyclus species in horses.. Vet Parasitol 2016;227:77–84.
    pubmed: 27523942
  35. Kooyman FNJ, Van Doorn D, Geurden T, Wagenaar J. Semi-quantitative differentiation of cyathostomin larval cultures by reverse line blot.. Vet Parasitol 2016;216:59–65.
    pubmed: 26801596
  36. Kuzmina TA, Kharchenko VO. Anthelmintic resistance in cyathostomins of brood horses in Ukraine and influence of anthelmintic treatments on strongylid community structure.. Vet Parasitol 2008;154:277–288.
    pubmed: 18485600
  37. Kuzmina TA, Dzeverin I, Kharchenko VA. Strongylids in domestic horses: influence of horse age, breed and deworming programs on the strongyle parasite community.. Vet Parasitol 2016;227:56–63.
    pubmed: 27523938
  38. Le Jambre L, Martin P, Johnston AJA PS. Efficacy of combination anthelmintics against multiple resistant strains of sheep nematodes.. Anim Prod Sci 2010;50:946–952.
  39. Lester H, Spanton J, Stratford C, Bartley D, Morgan E, Hodgkinson J, Coumbe K, Mair T, Swan B, Lemon G. Anthelmintic efficacy against cyathostomins in horses in Southern England.. Vet Parasitol 2013;197:189–196.
    pubmed: 23830687
  40. Lignon JS, Gonçalves NF, Cunha LL, Antunes TA, Leão MS, Camassola JLT, Pellegrin TG, Ripoll PK, Pappen FG, Pinto DM. Anthelmintic resistance in creole horses in the South of Rio Grande do Sul, Brazil.. Arq Bras Med Vet Zootec 2021;73:598–604.
  41. Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection.. Vet Parasitol 1999;85:113–121.
    pubmed: 10485358
  42. Lyons ET. 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(3):569–574.
    pubmed: 18931857
  43. Lyons ET, Tolliver SC. Further indication of lowered activity of ivermectin on immature small strongyles in the intestinal lumen of horses on a farm in Central Kentucky.. Parasitol Res 2013;112:889–891.
    pubmed: 22948206
  44. Lyons ET, Tolliver SC, Collins SS. Study (1991 to 2001) of drug-resistant Population B small strongyles in critical tests in horses in Kentucky at the termination of a 40-year investigation.. Parasitol Res 2007;101:689–701.
    pubmed: 17468973
  45. 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;109:1529–1535.
    pubmed: 21614543
  46. Lyons ET, Dorton AR, Tolliver SC. Evaluation of activity of fenbendazole, oxibendazole, piperazine , and pyrantel pamoate alone and combinations against ascarids, strongyles, and strongyloides in horse foals in field tests on two farms in Central Kentucky in 2014 and 2015.. Vet Parasitol Reg Stud 2016;3–4:23–26.
    pubmed: 31014495
  47. Macdonald SL, Abbas G, Ghafar A, Gauci CG, Bauquier J, El-Hage C, Tennent-Brown B, Wilkes EJA, Beasley A, Jacobson C, Cudmore L, Carrigan P, Hurley J, Beveridge I, Hughes KJ, Nielsen MK, Jabbar A. Egg reappearance periods of anthelmintics against equine cyathostomins: the state of play revisited.. Int J Parasitol Drugs Drug Resist 2023;21:28–39.
    pmc: PMC10105024pubmed: 36543048
  48. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads.. EMBnet J 2011;17:10–12.
  49. Martin F, Höglund J, Bergström TF, Karlsson Lindsjö O, Tydén E. Resistance to pyrantel embonate and efficacy of fenbendazole in Parascaris univalens on Swedish stud farms.. Vet Parasitol 2018;264:69–73.
    pubmed: 30503095
  50. Martins NS, Pinto DM, da Cunha LL, Lignon JS, dos Santos TC, Evaristo TA, Pappen FG, Nizoli LQ. Assessment of the efficacy of commercial anthelmintics in horses naturally infected with gastrointestinal nematodes.. Med Vet (UFRPE) 2021;15:28–32.
  51. Matthews JB. An update on cyathostomins: anthelmintic resistance and worm control.. Equine Vet Educ 2008;20:552–560.
  52. Matthews JB. Anthelmintic resistance in equine nematodes.. Int J Parasitol Drugs Drug Resist 2014;4:310–315.
    pmc: PMC4266799pubmed: 25516842
  53. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.. PLoS One 2013;8.
    pmc: PMC3632530pubmed: 23630581
  54. Mfitilodze MW, Hutchinson GW. Development of free-living stages of equine strongyles in faeces on pasture in a tropical environment.. Vet Parasitol 1988;26:285–296.
    pubmed: 3347989
  55. Mitchell CJ, O'Sullivan CM, Pinloche E, Wilkinson T, Morphew RM, McEwan NR. Using next-generation sequencing to determine diversity of horse intestinal worms: identifying the equine ‘nemabiome’.. J Equine Sci 2019;30:1–5.
    pmc: PMC6445754pubmed: 30944540
  56. Morris LH, Colgan S, Leathwick DM, Nielsen MK. Anthelmintic efficacy of single active and combination products against commonly occurring parasites in foals.. Vet Parasitol 2019;268:46–52.
    pubmed: 30981305
  57. Nielsen MK. Evidence-based considerations for control of Parascaris spp. infections in horses.. Equine Vet Educ 2016;28:224–231.
  58. Nielsen MK. Anthelmintic resistance in equine nematodes: current status and emerging trends.. Int J Parasitol Drugs Drug Resist 2022;20:76–88.
    pmc: PMC9630620pubmed: 36342004
  59. Nielsen MK, Kaplan RM, Thamsborg SM, Monrad J, Olsen SN. Climatic influences on development and survival of free-living stages of equine strongyles: implications for worm control strategies and managing anthelmintic resistance.. Vet J 2007;174:23–32.
    pubmed: 16815051
  60. Nielsen MK, Pfister K, von Samson-Himmelstjerna G. Selective therapy in equine parasite control—application and limitations.. Vet Parasitol 2014;202:95–103.
    pubmed: 24702770
  61. Nielsen M, Branan M, Wiedenheft A, Digianantonio R, Garber L, Kopral C, Phillippi-Taylor A, Traub-Dargatz J. Parasite control strategies used by equine owners in the United States: a national survey.. Vet Parasitol 2018;250:45–51.
    pubmed: 29329623
  62. Nielsen MK, Mittel L, Grice A, Erskine M, Graves E, Vaala W. AAEP Parasite Control Guidelines.. .
  63. Nielsen MK, Banahan M, Kaplan RM. Importation of macrocyclic lactone resistant cyathostomins on a US thoroughbred farm.. Int J Parasitol Drugs Drug Resist 2020;14:99–104.
    pmc: PMC7548974pubmed: 33022574
  64. Nielsen MK, Littman BA, Orzech SW, Ripley NE. Equine strongylids: ivermectin efficacy and fecal egg shedding patterns.. Parasitol Res 2022;121:1691–1697.
    pubmed: 35384503
  65. Nielsen MK, Steuer AE, Anderson HP, Gavriliuc S, Carpenter AB, Redman EM, Gilleard JS, Reinemeyer CR, Poissant J. Shortened egg reappearance periods of equine cyathostomins following ivermectin or moxidectin treatment: morphological and molecular investigation of efficacy and species composition.. Int J Parasitol 2022;52(12):787–798.
    pubmed: 36244428
  66. Nielsen MK, von Samson-Himmelstjerna G, Kuzmina TA, van Doorn DCK, Meana A, Rehbein S, Elliott T, Reinemeyer CR. World association for the advancement of veterinary parasitology (WAAVP): third edition of guideline for evaluating the efficacy of equine anthelmintics.. Vet Parasitol 2022;303.
    pubmed: 35164972
  67. Nielsen MK, Kaplan RM, Abbas G, Jabbar A. Biological implications of long-term anthelmintic treatment: what else besides resistance are we selecting for?. Trends Parasitol 2023;39:945–953.
    pubmed: 37633759
  68. O'Meara B, Mulcahy GJ VP. A survey of helminth control practices in equine establishments in Ireland.. Vet Parasitol 2002;109:101–110.
    pubmed: 12383629
  69. Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V. Scikit-learn: machine learning in Python.. J Mach Learn Res 2011;12:2825–2830.
  70. Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter?. Vet Parasitol 2014;201:1–8.
    pubmed: 24485565
  71. Poissant J, Gavriliuc S, Bellaw J, Redman EM, Avramenko RW, Robinson D, Workentine ML, Shury TK, Jenkins EJ, McLoughlin PD, Nielson MK, Gilleard JS. A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses.. Int J Parasitol 2021;51:183–192.
    pubmed: 33242465
  72. Pook JF, Power ML, Sangster NC, Hodgson JL, Hodgson DR. Evaluation of tests for anthelmintic resistance in cyathostomes.. Vet Parasitol 2002;106:331–343.
    pubmed: 12079739
  73. R Core Team. R: A Language and Environment for Statistical Computing.. .
  74. Reid S, Mair T, Hillyer M, Love S. Epidemiological risk factors associated with a diagnosis of clinical cyathostomiasis in the horse.. Equine Vet J 1995;27:127–130.
    pubmed: 7607145
  75. Reinemeyer CR. Anthelmintic resistance in non-strongylid parasites of horses.. Vet Parasitol 2012;185:9–15.
    pubmed: 22078748
  76. Reinemeyer CR, Prado JC, Nielsen MK. Comparison of the larvicidal efficacies of moxidectin or a five-day regimen of fenbendazole in horses harboring cyathostomin populations resistant to the adulticidal dosage of fenbendazole.. Vet Parasitol 2015;214:100–107.
    pubmed: 26477278
  77. Relf VE, Lester HE, Morgan ER, Hodgkinson JE, Matthews JB. Anthelmintic efficacy on UK Thoroughbred stud farms.. Int J Parasitol 2014;44:507–514.
    pubmed: 24746779
  78. Roeber F, Jex AR, Gasser RB. Comparative evaluation of two DNA isolation techniques for PCR-based diagnosis of gastrointestinal nematode infections in sheep.. Mol Cell Probes 2013;27:153–157.
    pubmed: 23524142
  79. Rolfe PF, Dawson KL. The efficacy of a combination anthelmintic against oxibendazole resistant small strongyles, large strongyles and ascarids in horses.. Aust Vet J 1994;71:304–306.
    pubmed: 7818443
  80. Rossano MG, Smith AR, Lyons ET. Shortened strongyle-type egg reappearance periods in naturally infected horses treated with moxidectin and failure of a larvicidal dose of fenbendazole to reduce fecal egg counts.. Vet Parasitol 2010;173:349–352.
    pubmed: 20675055
  81. Saeed MA, Beveridge I, Abbas G, Beasley A, Bauquier J, Wilkes E, Jacobson C, Hughes KJ, El-Hage C, O'Handley R, Hurley J, Cudmore L, Carrigan P, Walter L, Tennent-Brown B, Nielsen MK, Jabbar A. Systematic review of gastrointestinal nematodes of horses from Australia.. Parasites Vectors 2019;12:188.
    pmc: PMC6489199pubmed: 31036059
  82. Sallé G, Cortet J, Bois I, Dubès C, Guyot-Sionest Q, Larrieu C, Landrin V, Majorel G, Wittreck S, Woringer E. Risk factor analysis of equine strongyle resistance to anthelmintics.. Int J Parasitol Drugs Drug Resist 2017;7:407–415.
    pmc: PMC5727347pubmed: 29149701
  83. Sangster N. Pharmacology of anthelmintic resistance in cyathostomes: will it occur with the avermectin/milbemycins?. Vet Parasitol 1999;85:189–204.
    pubmed: 10485365
  84. Sargison N, Chambers A, Chaudhry U, Costa Júnior L, Doyle SR, Ehimiyein A, Evans M, Jennings A, Kelly R, Sargison F, Sinclair M, Zahid O. Faecal egg counts and nemabiome metabarcoding highlight the genomic complexity of equine cyathostomin communities and provide insight into their dynamics in a Scottish native pony herd.. Int J Parasitol 2022;52:763–774.
    pubmed: 36208676
  85. Scare JA, Lyons ET, Wielgus KM, Nielsen MK. Combination deworming for the control of double-resistant cyathostomin parasites – short and long term consequences.. Vet Parasitol 2018;251:112–118.
    pubmed: 29426466
  86. Scare JA, Leathwick DM, Sauermann CW, Lyons ET, Steuer AE, Jones BA, Clark M, Nielsen MK. Dealing with double trouble: combination deworming against double-drug resistant cyathostomins.. Int J Parasitol Drugs Drug Resist 2020;12:28–34.
    pmc: PMC7139983pubmed: 31883485
  87. Schougaard H, Nielsen MK. Apparent ivermectin resistance of Parascaris equorum in foals in Denmark.. Vet Rec 2007;160:439–440.
    pubmed: 17400903
  88. Torgerson PR, Paul M, Furrer R. Evaluating faecal egg count reduction using a specifically designed package “eggCounts” in R and a user friendly web interface.. Int J Parasitol 2014;44:299–303.
    pubmed: 24556564
  89. Traversa D, Castagna G, von Samson-Himmelstjerna G, Meloni S, Bartolini R, Geurden T, Pearce MC, Woringer E, Besognet B, Milillo P, D'Espois M. Efficacy of major anthelmintics against horse cyathostomins in France.. Vet Parasitol 2012;188:294–300.
    pubmed: 22538094
  90. van Doorn DC, Ploeger HW, Eysker M, Geurden T, Wagenaar JA, Kooyman FN. Cylicocyclus species predominate during shortened egg reappearance period in horses after treatment with ivermectin and moxidectin.. Vet Parasitol 2014;206:246–252.
    pubmed: 25458565
  91. von Samson-Himmelstjerna G. Anthelmintic resistance in equine parasites - detection, potential clinical relevance and implications for control.. Vet Parasitol 2012;185:2–8.
    pubmed: 22100141
  92. von Samson-Himmelstjerna G, Fritzen B, Demeler J, Schürmann S, Rohn K, Schnieder T, Epe C. Cases of reduced cyathostomin egg-reappearance period and failure of Parascaris equorum egg count reduction following ivermectin treatment as well as survey on pyrantel efficacy on German horse farms.. Vet Parasitol 2007;144:74–80.
    pubmed: 17112667
  93. Wang C, Torgerson PR, Kaplan RM, George MM, Furrer R. Modelling anthelmintic resistance by extending eggCounts package to allow individual efficacy.. Int J Parasitol Drugs Drug Resist 2018;8:386–393.
    pmc: PMC6091319pubmed: 30103206
  94. Wilkes E, McConaghy FF, Thompson RL, Dawson K, Sangster NC, Hughes KJ. Efficacy of a morantel-abamectin combination for the treatment of resistant ascarids in foals.. Aust Vet J 2017;95:85–88.
    pubmed: 28239856
  95. Wilkes EJA, Heller J, Raidal SL, Woodgate RG, Hughes KJ. A questionnaire study of parasite control in Thoroughbred and Standardbred horses in Australia.. Equine Vet J 2020;52:547–555.
    pubmed: 31725925
  96. Workentine ML, Chen R, Zhu S, Gavriliuc S, Shaw N, Rijke Jd, Redman EM, Avramenko RW, Wit J, Poissant J, Gilleard JS. A database for ITS2 sequences from nematodes.. BMC Genet 2020;21:74.
    pmc: PMC7350610pubmed: 32650716
  97. 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;8:42.
    pmc: PMC8001109pubmed: 33807857

Citations

This article has been cited 9 times.
  1. Varandas M, Lozano J, Agrícola R, Gomes L, Rosa T, Magalhães M, Lamas L, Rinaldi L, Oliveira M, Paz-Silva A, Madeira de Carvalho L. Comparing the Performance of McMaster, FLOTAC and Mini-FLOTAC Techniques in the Diagnosis of Strongylid Infections in Two Horse Populations in Portugal. Pathogens 2025 Oct 22;14(11).
    doi: 10.3390/pathogens14111075pubmed: 41305313google 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. Wang T, Chen X, Yan X, Su Y, Gao W, Liu C, Wang W. Progress in serology and molecular biology of equine parasite diagnosis: sustainable control strategies. Front Vet Sci 2025;12:1663577.
    doi: 10.3389/fvets.2025.1663577pubmed: 40979365google scholar: lookup
  4. Nielsen MK, Pyatt A, Perrett J, Tydén E, van Doorn D, Pihl TH, Schmidt JS, von Samson-Himmelstjerna G, Beasley A, Abbas G, Jabbar A. Global equine parasite control guidelines: Consensus or confusion?. Int J Parasitol Drugs Drug Resist 2025 Aug;28:100600.
    doi: 10.1016/j.ijpddr.2025.100600pubmed: 40472642google scholar: lookup
  5. Beasley A, Abbas G, Hughes K, El-Hage C, Jacobson C, Bauquier J, Wilkes E, Carrigan P, Cudmore L, Hurley J, Beveridge I, Nielsen M, Jabbar A. Australian guidelines for equine internal parasite management. Aust Vet J 2025 Apr;103(4):151-158.
    doi: 10.1111/avj.13424pubmed: 39837536google scholar: lookup
  6. Bull KE, Hodgkinson J, Allen K, Poissant J, Peachey LE. Quantitative DNA metabarcoding reveals species composition of a macrocyclic lactone and pyrantel resistant cyathostomin population in the UK. Int J Parasitol Drugs Drug Resist 2025 Apr;27:100576.
    doi: 10.1016/j.ijpddr.2024.100576pubmed: 39778419google scholar: lookup
  7. Hamad MH, Jitsamai W, Chinkangsadarn T, Ngangam TS, Wattanapornpilom T, Naraporn D, Ouisuwan S, Taweethavonsawat P. Prevalence, risk factors, and species diversity of strongylid nematodes in domesticated Thai horses: insights from ITS-2 rDNA metabarcoding. Parasitol Res 2024 Dec 17;123(12):410.
    doi: 10.1007/s00436-024-08438-0pubmed: 39688721google scholar: lookup
  8. Kuzmina TA, Königová A, Antipov A, Kuzmin Y, Kharchenko V, Syrota Y. Changes in equine strongylid communities after two decades of annual anthelmintic treatments at the farm level. Parasitol Res 2024 Nov 25;123(11):394.
    doi: 10.1007/s00436-024-08417-5pubmed: 39585485google scholar: lookup
  9. 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
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