FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Animals (Basel) / Patterns of Equine Small Strongyle Species Infection after I...
Animals : an open access journal from MDPI2024; 14(4); 574; doi: 10.3390/ani14040574

Patterns of Equine Small Strongyle Species Infection after Ivermectin Intervention in Thailand: Egg Reappearance Period and Nemabiome Metabarcoding Approach.

Abstract: The indiscriminate use of anthelmintics to control parasitic nematodes in horses has led to the emergence of anthelmintic resistance worldwide. However, there are no data available on using ivermectin for treating strongyle infections within domesticated horses in Thailand. Therefore, this study aimed to use the fecal egg count reduction (FECR) test to determine the strongylid egg reappearance period (ERP). Additionally, the nemabiome metabarcoding approach is incorporated to study patterns of strongyle species infection following ivermectin treatment. The study results indicate that, although ivermectin effectively eliminated adult strongyle parasites within two weeks post-treatment, the ERP was shortened to 6 weeks post-treatment with a mean FECR of 70.4% (95% CI 46.1-84.0). This potentially indicates a recent change in drug performance. In addition, nemabiome metabarcoding revealed that strongyle species have different levels of susceptibility in response to anthelmintic drugs. The reduction in ERP was associated with the early reappearance of specific species, dominated by and , indicating the lower susceptibility of these species. In contrast, , , and were not found post-treatment, indicating the high level of susceptibility of these species. This information is vital for comprehending the factors contributing to the emergence of resistance and for devising strategies to manage and control strongyle infections in horses.
Get Full Text
Publication Date: 2024-02-08 PubMed ID: 38396542PubMed Central: PMC10886017DOI: 10.3390/ani14040574Google 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.
LinkedInCopy
  • Journal Article

Cite This Article

APA
Hamad MH, Islam SI, Jitsamai W, Chinkangsadarn T, Naraporn D, Ouisuwan S, Taweethavonsawat P. (2024). Patterns of Equine Small Strongyle Species Infection after Ivermectin Intervention in Thailand: Egg Reappearance Period and Nemabiome Metabarcoding Approach. Animals (Basel), 14(4), 574. https://doi.org/10.3390/ani14040574

Publication

Animals : an open access journal from MDPI
ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 14
Issue: 4
PII: 574

Researcher Affiliations

Hamad, Mohamed H
  • The International Graduate Program of Veterinary Science and Technology (VST), Faculty of Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand.
  • Department of Animal Infectious Diseases, Faculty of Veterinary Medicine, Zagazig University, Zagazig 44511, Egypt.
  • Parasitology Unit, Department of Veterinary Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand.
Islam, Sk Injamamul
  • The International Graduate Program of Veterinary Science and Technology (VST), Faculty of Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand.
  • Parasitology Unit, Department of Veterinary Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand.
Jitsamai, Wanarit
  • Department of Parasitology and Entomology, Faculty of Public Health, Mahidol University, Bangkok 10400, Thailand.
Chinkangsadarn, Teerapol
  • Department of Surgery, Faculty of Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand.
Naraporn, Darm
  • Horse Farm and Laboratory Animal Breeding Center, Queen Saovabha Memorial Institute, The Thai Red Cross Society, Hua-Hin 77110, Thailand.
Ouisuwan, Suraseha
  • Horse Farm and Laboratory Animal Breeding Center, Queen Saovabha Memorial Institute, The Thai Red Cross Society, Hua-Hin 77110, Thailand.
Taweethavonsawat, Piyanan
  • Parasitology Unit, Department of Veterinary Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand.
  • Biomarkers in Animals Parasitology Research Unit, Chulalongkorn University, Bangkok 10330, Thailand.

Grant Funding

  • FOODF67310022 / Thailand Science Research and Innovation Fund

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 82 references
  1. Lichtenfels J.R., Kharchenko V.A., Dvojnos G.M. Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae) Vet. Parasitol. 2008;156:4–161. doi: 10.1016/j.vetpar.2008.04.026.
    doi: 10.1016/j.vetpar.2008.04.026pubmed: 18603375google scholar: lookup
  2. Kuzmina T., Kornas S., Basiaga M., Kharchenko V., Vyniarska A. Biodiversity of strongylids (Nematoda: Strongylidae) communities in domestic horses from Poland and Ukraine. Helminthologia. 2011;48:77–84. doi: 10.2478/s11687-011-0013-7.
    doi: 10.2478/s11687-011-0013-7google scholar: lookup
  3. Matthews J. An update on cyathostomins: Anthelmintic resistance and worm control. Equine Vet. Educ. 2008;20:552–560. doi: 10.2746/095777308X363912.
    doi: 10.2746/095777308X363912google scholar: lookup
  4. Kuzmina T.A., Dzeverin I., Kharchenko V.A. Strongylids in domestic horses: Influence of horse age, breed and deworming programs on the strongyle parasite community. Vet. Parasitol. 2016;227:56–63. doi: 10.1016/j.vetpar.2016.07.024.
    doi: 10.1016/j.vetpar.2016.07.024pubmed: 27523938google scholar: lookup
  5. Lyons E.T., Tolliver S.C., Drudge J.H. Historical perspective of cyathostomes: Prevalence, treatment and control programs. Vet. Parasitol. 1999;85:97–111; discussion 111–112, 215–225. doi: 10.1016/S0304-4017(99)00091-6.
    doi: 10.1016/S0304-4017(99)00091-6pubmed: 10485357google scholar: lookup
  6. Bredtmann C.M., Krucken 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. doi: 10.3389/fcimb.2017.00283.
    doi: 10.3389/fcimb.2017.00283pmc: PMC5487379pubmed: 28702376google scholar: lookup
  7. Bredtmann C.M., Krucken J., Murugaiyan J., Balard A., Hofer H., Kuzmina T.A., von Samson-Himmelstjerna G. Concurrent proteomic fingerprinting and molecular analysis of cyathostomins. Proteomics. 2019;19:e1800290. doi: 10.1002/pmic.201800290.
    doi: 10.1002/pmic.201800290pubmed: 30786147google scholar: lookup
  8. Bellaw J.L., Nielsen M.K. Meta-analysis of cyathostomin species-specific prevalence and relative abundance in domestic horses from 1975–2020: Emphasis on geographical region and specimen collection method. Parasit. Vectors. 2020;13:509. doi: 10.1186/s13071-020-04396-5.
    doi: 10.1186/s13071-020-04396-5pmc: PMC7552500pubmed: 33046130google scholar: lookup
  9. Love S., Murphy D., Mellor D. Pathogenicity of cyathostome infection. Vet. Parasitol. 1999;85:113–121; discussion 121–2, 215–25. doi: 10.1016/S0304-4017(99)00092-8.
    doi: 10.1016/S0304-4017(99)00092-8pubmed: 10485358google scholar: lookup
  10. Salem S.E., Abd El-Ghany A.M., Hamad M.H., Abdelaal A.M., Elsheikh H.A., Hamid A.A., Saud M.A., Daniels S.P., Ras R. Prevalence of gastrointestinal nematodes, parasite control practices and anthelmintic resistance patterns in a working horse population in Egypt. Equine Vet. J. 2021;53:339–348. doi: 10.1111/evj.13325.
    doi: 10.1111/evj.13325pubmed: 32725717google scholar: lookup
  11. Duncan J., Bairden K., Abbott E. Elimination of mucosal cyathostome larvae by five daily treatments with fenbendazole. Vet. Rec. 1998;142:268–271. doi: 10.1136/vr.142.11.268.
    doi: 10.1136/vr.142.11.268pubmed: 9569480google scholar: lookup
  12. Malan F.S., Reinecke R.K., Scialdo R.C. Anthelmintic efficacy fenbendazole paste in equines. J. S. Afr. Vet. Assoc. 1981;52:127–130.
    pubmed: 7277372
  13. Lyons E., Drudge J., Tolliver S. Critical tests of three salts of pyrantel against internal parasites of the horse. Am. J. Vet. Res. 1975;35:1515–1522.
    pubmed: 4279571
  14. Slocombe J.O., Smart J. Evaluation of pyrantel pamoate against strongyles in horses. Can. Vet. J. 1975;16:310–312.
    pmc: PMC1697063pubmed: 1192342
  15. Traversa D. The little-known scenario of anthelmintic resistance in equine cyathostomes in Italy. Ann. N. Y. Acad. Sci. 2008;1149:167–169. doi: 10.1196/annals.1428.078.
    doi: 10.1196/annals.1428.078pubmed: 19120201google scholar: lookup
  16. Brady H.A., Nichols W.T. Drug resistance in equine parasites: An emerging global problem. J. Equine Vet. Sci. 2009;29:285–295. doi: 10.1016/j.jevs.2009.04.186.
    doi: 10.1016/j.jevs.2009.04.186google scholar: lookup
  17. 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. doi: 10.1016/j.vetpar.2014.01.004.
    doi: 10.1016/j.vetpar.2014.01.004pubmed: 24485565google scholar: lookup
  18. Nielsen M.K., Steuer A.E., Anderson H.P., Gavriliuc S., Carpenter A.B., Redman E.M., Gilleard J.S., Reinemeyer C.R., 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;52:787–798. doi: 10.1016/j.ijpara.2022.09.003.
    doi: 10.1016/j.ijpara.2022.09.003pubmed: 36244428google scholar: lookup
  19. Kuzmina T.A., Zvegintsova N.S., Yasyntelska N.I., Kharchenko V.A. Anthelmintic resistance in strongylids (Nematoda: Strongylidae) parasitizing wild and domestic equids in the Askania Nova Biosphere Reserve, Ukraine. Ann. Parasitol. 2020;66:49–60. doi: 10.17420/ap6601.237.
    doi: 10.17420/ap6601.237pubmed: 32198995google scholar: lookup
  20. Relf V.E., Morgan E.R., Hodgkinson J.E., Matthews J.B. A questionnaire study on parasite control practices on UK breeding Thoroughbred studs. Equine Vet. J. 2012;44:466–471. doi: 10.1111/j.2042-3306.2011.00493.x.
    doi: 10.1111/j.2042-3306.2011.00493.xpubmed: 22050130google scholar: lookup
  21. Nielsen M.K., Monrad J., Olsen S.N. Prescription-only anthelmintics--a questionnaire survey of strategies for surveillance and control of equine strongyles in Denmark. Vet. Parasitol. 2006;135:47–55. doi: 10.1016/j.vetpar.2005.10.020.
    doi: 10.1016/j.vetpar.2005.10.020pubmed: 16309841google scholar: lookup
  22. Bellaw J.L., Krebs K., Reinemeyer C.R., Norris J.K., Scare J.A., Pagano S., Nielsen M.K. Anthelmintic therapy of equine cyathostomin nematodes–larvicidal efficacy, egg reappearance period, and drug resistance. Int. J. Parasitol. 2018;48:97–105. doi: 10.1016/j.ijpara.2017.08.009.
    doi: 10.1016/j.ijpara.2017.08.009pubmed: 29050919google scholar: lookup
  23. Elghryani N., McOwan T., Mincher C., Duggan V., de Waal T. Estimating the prevalence and factors affecting the shedding of helminth eggs in Irish equine populations. Animals. 2023;13:581. doi: 10.3390/ani13040581.
    doi: 10.3390/ani13040581pmc: PMC9951768pubmed: 36830368google scholar: lookup
  24. Alm Y.H., Osterman-Lind E., Martin F., Lindfors R., Roepstorff N., Hedenstrom U., Fredriksson I., Halvarsson P., Tyden E. Retained efficacy of ivermectin against cyathostomins in Swedish horse establishments practicing selective anthelmintic treatment. Vet. Parasitol. 2023;322:110007. doi: 10.1016/j.vetpar.2023.110007.
    doi: 10.1016/j.vetpar.2023.110007pubmed: 37639919google scholar: lookup
  25. Khan S., Nisar A., Yuan J., Luo X., Dou X., Liu F., Zhao X., Li J., Ahmad H., Mehmood S.A., et al. A whole genome re-sequencing based GWA analysis reveals candidate genes associated with ivermectin resistance in Haemonchus contortus. Genes. 2020;11:367. doi: 10.3390/genes11040367.
    doi: 10.3390/genes11040367pmc: PMC7230667pubmed: 32231078google scholar: lookup
  26. Robert M., Hu W., Nielsen M., Stowe C. 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. doi: 10.1111/evj.12344.
    doi: 10.1111/evj.12344pubmed: 25196091google scholar: lookup
  27. Raza A., Qamar A.G., Hayat K., Ashraf S., Williams A.R. Anthelmintic resistance and novel control options in equine gastrointestinal nematodes. Parasitology. 2019;146:425–437. doi: 10.1017/S0031182018001786.
    doi: 10.1017/S0031182018001786pubmed: 30392477google scholar: lookup
  28. Lyons E.T., Tolliver S.C., Ionita M., Lewellen A., Collins S.S. Field studies indicating reduced activity of ivermectin on small strongyles in horses on a farm in Central Kentucky. Parasitol. Res. 2008;103:209–215. doi: 10.1007/s00436-008-0959-7.
    doi: 10.1007/s00436-008-0959-7pubmed: 18389281google scholar: lookup
  29. Lyons E., Tolliver S. 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. doi: 10.1007/s00436-012-3098-0.
    doi: 10.1007/s00436-012-3098-0pubmed: 22948206google scholar: lookup
  30. Coles G., Bauer C., Borgsteede F., Geerts S., Klei T., Taylor M., Waller P. World Association for the Advancement of Veterinary Parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 1992;44:35–44. doi: 10.1016/0304-4017(92)90141-U.
    doi: 10.1016/0304-4017(92)90141-Upubmed: 1441190google scholar: lookup
  31. Kaplan R.M., Denwood M.J., Nielsen M.K., Thamsborg S.M., Torgerson P.R., Gilleard J.S., Dobson R.J., 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;318:109936. doi: 10.1016/j.vetpar.2023.109936.
    doi: 10.1016/j.vetpar.2023.109936pubmed: 37121092google scholar: lookup
  32. Sangster N.C. Pharmacology of anthelmintic resistance in cyathostomes: Will it occur with the avermectin/milbemycins? Vet. Parasitol. 1999;85:189–201; discussion 201–4, 215–25. doi: 10.1016/S0304-4017(99)00099-0.
    doi: 10.1016/S0304-4017(99)00099-0pubmed: 10485365google scholar: lookup
  33. Nielsen M.K. Anthelmintic resistance in equine nematodes: Current status and emerging trends. Int. J. Parasitol. Drugs Drug Resist. 2022;20:76–88. doi: 10.1016/j.ijpddr.2022.10.005.
    doi: 10.1016/j.ijpddr.2022.10.005pmc: PMC9630620pubmed: 36342004google scholar: lookup
  34. Nielsen M.K., von Samson-Himmelstjerna G., Kuzmina T.A., van Doorn D.C.K., Meana A., Rehbein S., Elliott T., Reinemeyer C.R. World association for the advancement of veterinary parasitology (WAAVP): Third edition of guideline for evaluating the efficacy of equine anthelmintics. Vet. Parasitol. 2022;303:109676. doi: 10.1016/j.vetpar.2022.109676.
    doi: 10.1016/j.vetpar.2022.109676pubmed: 35164972google scholar: lookup
  35. Buono F., Roncoroni C., Pacifico L., Piantedosi D., Neola B., Barile V.L., Fagiolo A., Várady M., Veneziano V. Cyathostominae egg reappearance period after treatment with major horse anthelmintics in donkeys. J. Equine Vet. Sci. 2018;65:6–11. doi: 10.1016/j.jevs.2018.02.018.
    doi: 10.1016/j.jevs.2018.02.018google scholar: lookup
  36. Demeulenaere D., Vercruysse J., Dorny P., Claerebout E. Comparative studies of ivermectin and moxidectin in the control of naturally acquired cyathostome infections in horses. Vet. Rec. 1997;141:383–386. doi: 10.1136/vr.141.15.383.
    doi: 10.1136/vr.141.15.383pubmed: 9364706google scholar: lookup
  37. Piche C.A., Kennedy M.J., Herbers H.A., Newcomb K.M. Comparison of ivermectin, oxibendazole, and pyrantel pamoate in suppressing fecal egg output in horses. Can. Vet. J. 1991;32:104–107.
    pmc: PMC1480944pubmed: 17423731
  38. Porr C.A.S., Hedinger V.F., Hamm L.R., Ernst M.M., Papajeski B.M., Santiago M.L., Davis A.J. Effects of ivermectin and moxidectin on fecal egg count and egg reappearance rate in horses. J. Equine Vet. Sci. 2017;57:51–55. doi: 10.1016/j.jevs.2017.06.011.
    doi: 10.1016/j.jevs.2017.06.011google scholar: lookup
  39. Baranova M.V., Panova O.A., Polukhina D.N., Panova D.S. Reduction of the nematode egg reappearance period in horses after anthelmintic therapy. Vet. World. 2022;15:1530–1534. doi: 10.14202/vetworld.2022.1530-1534.
    doi: 10.14202/vetworld.2022.1530-1534pmc: PMC9375206pubmed: 35993067google scholar: lookup
  40. Corning S. Equine cyathostomins: A review of biology, clinical significance and therapy. Parasit. Vectors. 2009;2((Suppl. S2)):S1. doi: 10.1186/1756-3305-2-S2-S1.
    doi: 10.1186/1756-3305-2-S2-S1pmc: PMC2751837pubmed: 19778462google scholar: lookup
  41. Johnson A.C.B., Biddle A.S. The use of molecular profiling to track equine reinfection rates of cyathostomin species following anthelmintic administration. Animals. 2021;11:1345. doi: 10.3390/ani11051345.
    doi: 10.3390/ani11051345pmc: PMC8150961pubmed: 34065099google scholar: lookup
  42. Molena R.A., Peachey L.E., Di Cesare A., Traversa D., Cantacessi C. Cyathostomine egg reappearance period following ivermectin treatment in a cohort of UK Thoroughbreds. Parasit. Vectors. 2018;11:61. doi: 10.1186/s13071-018-2638-6.
    doi: 10.1186/s13071-018-2638-6pmc: PMC5785887pubmed: 29370872google scholar: lookup
  43. Sargison N., Chambers A., Chaudhry U., Júnior L.C., Doyle S.R., Ehimiyein A., Evans M., Jennings A., Kelly R., Sargison F. 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. doi: 10.1016/j.ijpara.2022.08.002.
    doi: 10.1016/j.ijpara.2022.08.002pubmed: 36208676google scholar: lookup
  44. Poissant J., Gavriliuc S., Bellaw J., Redman E.M., Avramenko R.W., Robinson D., Workentine M.L., Shury T.K., Jenkins E.J., McLoughlin P.D., et al. A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses. Int. J. Parasitol. 2021;51:183–192. doi: 10.1016/j.ijpara.2020.09.003.
    doi: 10.1016/j.ijpara.2020.09.003pubmed: 33242465google scholar: lookup
  45. Avramenko R.W., Bras A., Redman E.M., Woodbury M.R., Wagner B., Shury T., Liccioli S., Windeyer M.C., Gilleard J.S. High species diversity of trichostrongyle parasite communities within and between Western Canadian commercial and conservation bison herds revealed by nemabiome metabarcoding. Parasit. Vectors. 2018;11:299. doi: 10.1186/s13071-018-2880-y.
    doi: 10.1186/s13071-018-2880-ypmc: PMC5952520pubmed: 29764472google scholar: lookup
  46. Pafco B., Cizkova D., Kreisinger J., Hasegawa H., Vallo P., Shutt K., Todd A., Petrzelkova K.J., Modry D. Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Sci. Rep. 2018;8:5933. doi: 10.1038/s41598-018-24126-3.
    doi: 10.1038/s41598-018-24126-3pmc: PMC5897349pubmed: 29651122google scholar: lookup
  47. van Wyk J.A. Refugia-overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort J. Vet. 2001;68:55–67.
    pubmed: 11403431
  48. Lester H.E., Morgan E.R., Hodgkinson J.E., Matthews J.B. Analysis of strongyle egg shedding consistency in horses and factors that affect it. J. Equine Vet. Sci. 2018;60:113–119.e1. doi: 10.1016/j.jevs.2017.04.006.
    doi: 10.1016/j.jevs.2017.04.006google scholar: lookup
  49. 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. Online at American Association of Equine Practitioners. 2019. [(accessed on 1 December 2020)]. Available online: www.aaep.org.
  50. Dias de Castro L.L., Abrahão C.L.H., Buzatti A., Molento M.B., Bastianetto E., Rodrigues D.S., Lopes L.B., Silva M.X., de Freitas M.G., Conde M.H., et al. Comparison of McMaster and Mini-FLOTAC fecal egg counting techniques in cattle and horses. Vet. Parasitol. Reg. Stud. Rep. 2017;10:132–135. doi: 10.1016/j.vprsr.2017.10.003.
    doi: 10.1016/j.vprsr.2017.10.003pubmed: 31014585google scholar: lookup
  51. Anonymous. Manual of Veterinary Parasitological Laboratory Techniques. 3rd ed. Ministry of Agriculture Fisheries and Food; London, UK: 1986. p. 160. Ref. Book 418.
  52. Gasser R.B., Chilton N.B., Hoste H., Beveridge I. Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Res. 1993;21:2525–2526. doi: 10.1093/nar/21.10.2525.
    doi: 10.1093/nar/21.10.2525pmc: PMC309567pubmed: 8506152google scholar: lookup
  53. Boisseau M., Dhorne-Pollet S., Bars-Cortina D., Courtot É., Serreau D., Annonay G., Lluch J., Gesbert A., Reigner F., Sallé G. Species interactions, stability, and resilience of the gut microbiota-helminth assemblage in horses. iScience. 2023;26:106044. doi: 10.1016/j.isci.2023.106044.
    doi: 10.1016/j.isci.2023.106044pmc: PMC9929684pubmed: 36818309google scholar: lookup
  54. Jalili V., Afgan E., Gu Q., Clements D., Blankenberg D., Goecks J., Taylor J., Nekrutenko A. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2020 update. Nucleic Acids Res. 2020;48:W395–W402. doi: 10.1093/nar/gkaa434.
    doi: 10.1093/nar/gkaa434pmc: PMC7319590pubmed: 32479607google scholar: lookup
  55. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 2011;17:10–12. doi: 10.14806/ej.17.1.200.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  56. Callahan B.J., McMurdie P.J., Rosen M.J., Han A.W., Johnson A.J., Holmes S.P. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869.
    doi: 10.1038/nmeth.3869pmc: PMC4927377pubmed: 27214047google scholar: lookup
  57. Bengtsson-Palme J., Ryberg M., Hartmann M., Branco S., Wang Z., Godhe A., De Wit P., Sánchez-García M., Ebersberger I., de Sousa F. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 2013;4:914–919. doi: 10.1111/2041-210X.12073.
    doi: 10.1111/2041-210X.12073google scholar: lookup
  58. Wright E.S., Vetsigian K.H. Quality filtering of Illumina index reads mitigates sample cross-talk. BMC Genom. 2016;17:876. doi: 10.1186/s12864-016-3217-x.
    doi: 10.1186/s12864-016-3217-xpmc: PMC5097354pubmed: 27814679google scholar: lookup
  59. Avramenko R.W., Redman E.M., Lewis R., Yazwinski T.A., Wasmuth J.D., Gilleard J.S. Exploring the gastrointestinal “Nemabiome”: Deep amplicon sequencing to quantify the species composition of parasitic nematode communities. PLoS ONE. 2015;10:e0143559. doi: 10.1371/journal.pone.0143559.
    doi: 10.1371/journal.pone.0143559pmc: PMC4668017pubmed: 26630572google scholar: lookup
  60. Denwood M.J., Kaplan R.M., McKendrick I.J., Thamsborg S.M., Nielsen M.K., 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;314:109867. doi: 10.1016/j.vetpar.2022.109867.
    doi: 10.1016/j.vetpar.2022.109867pubmed: 36621042google scholar: lookup
  61. Torgerson P.R., 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. doi: 10.1016/j.ijpara.2014.01.005.
    doi: 10.1016/j.ijpara.2014.01.005pubmed: 24556564google scholar: lookup
  62. Wang C., Torgerson P.R., Kaplan R.M., George M.M., Furrer R. Modelling anthelmintic resistance by extending eggCounts package to allow individual efficacy. Int. J. Parasitol. Drugs Drug Resist. 2018;8:386–393. doi: 10.1016/j.ijpddr.2018.07.003.
    doi: 10.1016/j.ijpddr.2018.07.003pmc: PMC6091319pubmed: 30103206google scholar: lookup
  63. Wickham H. Getting Started with ggplot2. In: Wickham H., editor. ggplot2: Elegant Graphics for Data Analysis. Springer International Publishing; Cham, Switzerland: 2016. pp. 11–31.
  64. Oksanen J., Blanchet F.G., Friendly M., Kindt R., Legendre P., McGlinn D., Minchin P.R., O’Hara R.B., Simpson G.L., Solymos P. Community Ecology Package. [(accessed on 15 October 2023)]. Available online: https://cran.r-project.org/package=vegan.
  65. Hill M.O. Diversity and evenness: A unifying notation and its consequences. Ecology. 1973;54:427–432. doi: 10.2307/1934352.
    doi: 10.2307/1934352google scholar: lookup
  66. Shannon C.E. A mathematical theory of communication. Bell Syst. Tech. J. 1948;27:379–423. doi: 10.1002/j.1538-7305.1948.tb01338.x.
    doi: 10.1002/j.1538-7305.1948.tb01338.xgoogle scholar: lookup
  67. Fissiha W., Kinde M.Z. Anthelmintic resistance and its mechanism: A Review. Infect. Drug Resist. 2021;14:5403–5410. doi: 10.2147/IDR.S332378.
    doi: 10.2147/IDR.S332378pmc: PMC8687516pubmed: 34938088google scholar: lookup
  68. Dauparaite E., Kupcinskas T., von Samson-Himmelstjerna G., Petkevicius S. Anthelmintic resistance of horse strongyle nematodes to ivermectin and pyrantel in Lithuania. Acta Vet. Scand. 2021;63:5. doi: 10.1186/s13028-021-00569-z.
    doi: 10.1186/s13028-021-00569-zpmc: PMC7836172pubmed: 33494770google scholar: lookup
  69. Denwood M., Innocent G., Prentice J., Matthews L., Reid S., Pipper C., Levecke B., Kaplan R., Kotze A., Keiser J. A hypothesis testing framework for the ratio of means of two negative binomial distributions: Classifying the efficacy of anthelmintic treatment against intestinal parasites. arXiv. 20191910.06667
  70. Traversa D., von Samson-Himmelstjerna G., Demeler J., Milillo P., Schürmann S., Barnes H., Otranto D., Perrucci S., di Regalbono A.F., Beraldo P. Anthelmintic resistance in cyathostomin populations from horse yards in Italy, United Kingdom and Germany. Parasit. Vectors. 2009;2((Suppl. 2)):S2. doi: 10.1186/1756-3305-2-S2-S2.
    doi: 10.1186/1756-3305-2-S2-S2pmc: PMC2751838pubmed: 19778463google scholar: lookup
  71. Daniels S.P., Proudman C.J. Shortened egg reappearance after ivermectin or moxidectin use in horses in the UK. Vet. J. 2016;218:36–39. doi: 10.1016/j.tvjl.2016.11.003.
    doi: 10.1016/j.tvjl.2016.11.003pubmed: 27938707google scholar: lookup
  72. Hinney B., Wirtherle N.C., Kyule M., Miethe N., Zessin K.H., Clausen P.H. 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;109:1625–1635. doi: 10.1007/s00436-011-2434-0.
    doi: 10.1007/s00436-011-2434-0pubmed: 21559764google scholar: lookup
  73. 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. doi: 10.1016/j.vetpar.2017.12.012.
    doi: 10.1016/j.vetpar.2017.12.012pubmed: 29329623google scholar: lookup
  74. Saeed M.A., Beveridge I., Abbas G., Beasley A., Bauquier J., Wilkes E., Jacobson C., Hughes K.J., El-Hage C., O’Handley R., et al. Systematic review of gastrointestinal nematodes of horses from Australia. Parasit. Vectors. 2019;12:188. doi: 10.1186/s13071-019-3445-4.
    doi: 10.1186/s13071-019-3445-4pmc: PMC6489199pubmed: 31036059google scholar: lookup
  75. Larsen M.L., Ritz C., Petersen S.L., Nielsen M.K. Determination of ivermectin efficacy against cyathostomins and Parascaris equorum on horse farms using selective therapy. Vet. J. 2011;188:44–47. doi: 10.1016/j.tvjl.2010.03.009.
    doi: 10.1016/j.tvjl.2010.03.009pubmed: 20385508google scholar: lookup
  76. van Doorn D.C., Ploeger H.W., Eysker M., Geurden T., Wagenaar J.A., Kooyman F.N. Cylicocyclus species predominate during shortened egg reappearance period in horses after treatment with ivermectin and moxidectin. Vet. Parasitol. 2014;206:246–252. doi: 10.1016/j.vetpar.2014.10.004.
    doi: 10.1016/j.vetpar.2014.10.004pubmed: 25458565google scholar: lookup
  77. 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. doi: 10.1016/j.vetpar.2006.09.036.
    doi: 10.1016/j.vetpar.2006.09.036pubmed: 17112667google scholar: lookup
  78. Nielsen M.K. Sustainable equine parasite control: Perspectives and research needs. Vet. Parasitol. 2012;185:32–44. doi: 10.1016/j.vetpar.2011.10.012.
    doi: 10.1016/j.vetpar.2011.10.012pubmed: 22055611google scholar: lookup
  79. Steinbach T., Bauer C., Sasse H., Baumgartner W., Rey-Moreno C., Hermosilla C., Damriyasa I.M., Zahner H. Small strongyle infection: Consequences of larvicidal treatment of horses with fenbendazole and moxidectin. Vet. Parasitol. 2006;139:115–131. doi: 10.1016/j.vetpar.2006.03.028.
    doi: 10.1016/j.vetpar.2006.03.028pubmed: 16675126google scholar: lookup
  80. Seyoum Z., Tesfaye M., Derso S. Prevalence, intensity and risk factors of infestation with major gastrointestinal nematodes in equines in and around Shashemane, Southern Ethiopia. Trop. Anim. Health Prod. 2015;47:1515–1521. doi: 10.1007/s11250-015-0893-5.
    doi: 10.1007/s11250-015-0893-5pubmed: 26205906google scholar: lookup
  81. Lavoie J.P., Drolet R., Parsons D., Leguillette R., Sauvageau R., Shapiro J., Houle L., Halle G., Gebhart C.J. Equine proliferative enteropathy: A cause of weight loss, colic, diarrhoea and hypoproteinaemia in foals on three breeding farms in Canada. Equine Vet. J. 2000;32:418–425. doi: 10.2746/042516400777591110.
    doi: 10.2746/042516400777591110pubmed: 11037264google scholar: lookup
  82. Ionita M., Howe D.K., Lyons E.T., Tolliver S.C., Kaplan R.M., Mitrea I.L., Yeargan M. Use of a reverse line blot assay to survey small strongyle (Strongylida: Cyathostominae) populations in horses before and after treatment with ivermectin. Vet. Parasitol. 2010;168:332–337. doi: 10.1016/j.vetpar.2009.11.021.
    doi: 10.1016/j.vetpar.2009.11.021pubmed: 20045254google scholar: lookup

Citations

This article has been cited 3 times.
  1. Mohtasebi S, Ahn S, Karimi M, Saberi M, Gilleard JS, Poissant J. Enhanced detection of equine strongyles: Insights from morphological and nemabiome metabarcoding approaches in northern Iran.. Equine Vet J 2026 Mar;58(2):508-522.
    doi: 10.1111/evj.70120pubmed: 41316832google 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. 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
Subscribe to our newsletter
Join 99,001 horse owners like you who receive our email updates on horse health and nutrition.