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Parasitology research2024; 123(11); 394; doi: 10.1007/s00436-024-08417-5

Changes in equine strongylid communities after two decades of annual anthelmintic treatments at the farm level.

Abstract: The aim of this study was to assess the changes in strongylid communities of domestic horses after two decades of regular anthelmintic treatments; the changes in prevalence and relative abundance of individual strongylid species and their contribution to the observed alterations were estimated. The study was conducted in 2023; data collected in 2004 were used for comparison; 39 horses from two farms in Ukraine (22 horses in 2004 and 17 in 2023) were examined. In total, 18,999 strongylid specimens were collected by in vivo diagnostic deworming method before (in 2004, 9119 specimens) and after (in 2023, 9880 specimens) frequent application of anthelmintics. Strongylids were identified morphologically. Thirteen strongylid species were found in horses in 2023; only small strongylids (Cyathostominae) were recorded. In 2004, 21 species were found: 6 species of large strongylids (Strongylinae) and 15 of cyathostomins. Species richness (Margalef's index) and species diversity (Shannon's and Simpson's indexes) decreased over two decades on both farms; the Berger-Parker dominance index for C. nassatus dramatically increased up to 74.4. The dissimilarity of strongylid communities of 2023 and 2004 was primarily connected with the disappearance of large strongylids and rare cyathostomin species after two decades of regular anthelmintic treatments. SIMPER analysis revealed that C. nassatus and C. catinatum mostly contributed to this dissimilarity. A trend of gradual transformation of the strongylid community structure from multimodal (in 2004) to bimodal (in 2023) was observed on both farms.
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Publication Date: 2024-11-25 PubMed ID: 39585485PubMed Central: PMC11588933DOI: 10.1007/s00436-024-08417-5Google Scholar: Lookup
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  • Journal Article

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 study evaluates the shift in strongylid (a type of parasitic worm) populations in domestic horses following 20 years of regular anthelmintic (deworming) treatments, by comparing data from 2004 and 2023. The study noted a reduction in diversity of strongylid species and changes in the community structure of these parasites in horses over the two decades.

Methods and Study Setup

  • The research was conducted in 2023, using data collected in 2004 for comparison.
  • 39 horses from two farms in Ukraine were evaluated, with 22 horses in 2004 and 17 in 2023 studied separately.
  • A total of 18,999 strongylid samples were collected using an in vivo diagnostic deworming technique before and after consistent use of anthelmintics. In 2004 9119 specimens were examined and in 2023, 9880.
  • The parasites were identified morphologically for classification purposes.

Results and Observations

  • In 2023, thirteen strongylid species were found, all belonging to the smaller cyathostomins category.
  • In 2004, 21 species were identified, including six species of larger strongylids (Strongylinae) and 15 of cyathostomins.
  • The richness and diversity of species reduced over the two decades marked by the difference in Margalef’s, Shannon’s and Simpson’s indexes on both farms.
  • A significant increase of up to 74.4 in the Berger-Parker dominance index for C. nassatus, a specific cyathostomin species, was also observed.

Key Findings

  • The differences in the communities of strongylids in 2004 and 2023 were primarily linked to the extinction of larger strongylids and infrequent species of cyathostomins, linked to strict anthelmintic treatments over two decades.
  • SIMPER analysis showed that C. nassatus and C. catinatum significantly contributed to this disparity.
  • The structure of the strongylid community metamorphosed from multimodal in 2004, to bimodal in 2023 across both farms.

In general, the study offers evidence of significant changes in the parasite community within horses following the long-term use of anthelmintic treatments.

Cite This Article

APA
Kuzmina TA, Königová A, Antipov A, Kuzmin Y, Kharchenko V, Syrota Y. (2024). Changes in equine strongylid communities after two decades of annual anthelmintic treatments at the farm level. Parasitol Res, 123(11), 394. https://doi.org/10.1007/s00436-024-08417-5

Publication

Parasitology research
ISSN: 1432-1955
NlmUniqueID: 8703571
Country: Germany
Language: English
Volume: 123
Issue: 11
Pages: 394

Researcher Affiliations

Kuzmina, Tetiana A
  • Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Kosice, Slovakia. takuzmina@gmail.com.
  • I. I. Schmalhausen Institute of Zoology NAS of Ukraine, B. Khmelnytsky Street, 15, Kiev, Ukraine. takuzmina@gmail.com.
Königová, Alžbeta
  • Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Kosice, Slovakia.
Antipov, Anatoliy
  • Bila Tserkva National Agrarian University, Vul. Stavyshanska, 128, Bila Tserkva, Ukraine.
Kuzmin, Yuriy
  • I. I. Schmalhausen Institute of Zoology NAS of Ukraine, B. Khmelnytsky Street, 15, Kiev, Ukraine.
Kharchenko, Vitaliy
  • I. I. Schmalhausen Institute of Zoology NAS of Ukraine, B. Khmelnytsky Street, 15, Kiev, Ukraine.
Syrota, Yaroslav
  • Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, Kosice, Slovakia.
  • I. I. Schmalhausen Institute of Zoology NAS of Ukraine, B. Khmelnytsky Street, 15, Kiev, Ukraine.

MeSH Terms

  • Animals
  • Horses / parasitology
  • Anthelmintics / administration & dosage
  • Anthelmintics / therapeutic use
  • Ukraine
  • Farms
  • Horse Diseases / parasitology
  • Horse Diseases / drug therapy
  • Strongylida Infections / veterinary
  • Strongylida Infections / drug therapy
  • Strongylida Infections / parasitology
  • Strongylida Infections / epidemiology
  • Prevalence
  • Strongyloidea / drug effects
  • Strongyloidea / classification
  • Strongyloidea / isolation & purification
  • Biodiversity

Grant Funding

  • projects No. 09I03-03-V01-00015 and No. 09I03-03-V01-00046 / EU NextGenerationEU through the Recovery and Resilience Plan for Slovakia
  • projects No. 09I03-03-V01-00015 and No. 09I03-03-V01-00046 / EU NextGenerationEU through the Recovery and Resilience Plan for Slovakia

Conflict of Interest Statement

Declarations. Ethics approval and consent to participate: All national and institutional guidelines for the care and use of animals were followed. Consent for publication: Not applicable. Competing interests: The authors declare no competing interests.

References

This article includes 82 references
  1. 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. A national survey of anthelmintic resistance in ascarid and strongylid nematodes in Australian thoroughbred horses. Int J Parasitol Drugs Drug Resist 24:100517.
    pmc: PMC10757041pubmed: 38064906doi: 10.1016/j.ijpddr.2023.11.006google scholar: lookup
  2. Abbas G, Ghafar A, Beasley A, Stevenson MA, Bauquier J, Koehler AV, Wilkes EJA, McConnell E, El-Hage C, Carrigan P, Cudmore L, Hurley J, Gauci CG, Beveridge I, Jacobson C, Nielsen MK, Hughes KJ, Jabbar A. Understanding temporal and spatial distribution of intestinal nematodes of horses using faecal egg counts and DNA metabarcoding. Vet Parasitol 325:110094.
    pubmed: 38091893doi: 10.1016/j.vetpar.2023.110094google scholar: lookup
  3. Anjos DH, Rodrigues ML. Structure of the community of the Strongylidae nematodes in the dorsal colon of Equus caballus from Rio de Janeiro state – Brazil. Vet Parasitol 112:109–116.
    pubmed: 12581589doi: 10.1016/s0304-4017(02)00424-7google scholar: lookup
  4. 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. Parasit Vectors 13(1):509.
    pmc: PMC7552500pubmed: 33046130doi: 10.1186/s13071-020-04396-5google scholar: lookup
  5. 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 122:749–767.
    pmc: PMC9988789pubmed: 36627515doi: 10.1007/s00436-022-07765-4google scholar: lookup
  6. Boisseau M, Mach N, Basiaga M, Kuzmina T, Laugier C, Sallé G. Patterns of variation in equine strongyle community structure across age groups and gut compartments. Parasites Vectors 16:64.
    pmc: PMC9921056pubmed: 36765420doi: 10.1186/s13071-022-05645-5google scholar: lookup
  7. Bredtmann CM, Krücken J, Kuzmina T, Louro M, Madeira de Carvalho LM, von Samson-Himmelstjerna G. Nuclear and mitochondrial marker sequences reveal close relationship between Coronocyclus coronatus and a potential Cylicostephanus calicatus cryptic species complex. Infect Genet Evol 75:103956.
    pubmed: 31299325doi: 10.1016/j.meegid.2019.103956google scholar: lookup
  8. Breheny P, Burchett W. Visualization of regression models using visreg. The R Journal 9:56–71.
    doi: 10.32614/rj-2017-046google scholar: lookup
  9. Bucknell D, Hoste H, Gasser RB, Beveridge I. The structure of the community of strongyloid nematodes of domestic equids. J Helminthol 70:185–192.
    pubmed: 8960216doi: 10.1017/s0022149x0001539xgoogle scholar: lookup
  10. Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583.
    pubmed: 9267395doi: 10.2307/3284227google scholar: lookup
  11. Chapman MR, French DD, Klei TR. Gastrointestinal helminths of ponies in Louisiana: a comparison of species currently prevalent with those present 20 years ago. J Parasitol 88(6):1130–1134.
    pubmed: 12537106doi: 10.1645/0022-3395(2002)088[1130:ghopil]2.0.co;2google scholar: lookup
  12. Cirak VY, Hermosilla C, Bauer C. Study on the gastrointestinal parasite fauna of ponies in northern Germany. Appl Parasitol 37:239–244.
    pubmed: 9060170
  13. Clarke KR, Gorley RN. PRIMER v6: user manual/tutorial (plymouth routines in multivariate ecological research). .
  14. 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 11:e15124.
    pmc: PMC10105562pubmed: 37070089doi: 10.7717/peerj.15124google scholar: lookup
  15. Dorai-Raj S. binom: binomial confidence intervals for several parameterizations (Version 1.1–1.1) [R package]. CRAN .
  16. Drudge JH, Lyons ET. Control of internal parasites of horses. J Am Vet Med Assoc 148:378–383.
    pubmed: 5950040
  17. Halvarsson P, Grandi G, Hägglund S, Höglund J. Gastrointestinal parasite community structure in horses after the introduction of selective anthelmintic treatment strategies. Vet Parasitol 326:110111.
    pubmed: 38218052doi: 10.1016/j.vetpar.2023.110111google scholar: lookup
  18. Hammer Ø. PAST, paleontological statistics, Version 3.10, Reference Manual. .
  19. Herd RP. The changing world of worms—the rise of the cyathostomes and the decline of Strongylus vulgaris. Com Cont Educ Pract Vet 12:732–736.
  20. Herd RP. Performing equine fecal egg counts. Vet Med 87:240–244.
  21. Hinney B, Wirtherle NC, Kyule M, Miethe N, Zessin KH, Clausen PH. Prevalence of helminths in horses in the state of Brandenburg, Germany. Parasitol Res 108:1083–1091.
    pubmed: 21472400doi: 10.1007/s00436-011-2362-zgoogle scholar: lookup
  22. Hodgkinson JE, Kaplan RM, Kenyon F, Morgan ER, Park AW, Paterson S, Babayan SA, Beesley NJ, Britton C, Chaudhry U, Doyle SR, Ezenwa VO, Fenton A, Howell SB, Laing R, Mable BK, Matthews L, McIntyre J, Milne CE, Morrison TA, Prentice JC, Sargison ND, Williams DJL, Wolstenholme AJ, Devaney E. Refugia and anthelmintic resistance: concepts and challenges. Int J Parasitol Drugs Drug Resist 10:51–57.
    pmc: PMC6531808pubmed: 31125837doi: 10.1016/j.ijpddr.2019.05.001google scholar: lookup
  23. Hung G-C, Chilton NB, Beveridge I, Zhu XQ, Lichtenfels JR, Gasser RB. Molecular evidence for cryptic species within Cylicostephanus minutus (Nematoda: Strongylidae). Int J Parasitol 29:285–291.
    pubmed: 10221629doi: 10.1016/s0020-7519(98)00203-3google scholar: lookup
  24. 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 9:892920.
    pmc: PMC9226773pubmed: 35754549doi: 10.3389/fvets.2022.892920google scholar: lookup
  25. Kaplan RM. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol 20:477–481.
    pubmed: 15363441doi: 10.1016/j.pt.2004.08.001google scholar: lookup
  26. Kaplan RM, Nielsen MK. An evidence-based approach to equine parasite control: it ain’t the 60s anymore. Equine Vet Educ 22:306–316.
    doi: 10.1111/j.2042-3292.2010.00084.xgoogle scholar: lookup
  27. Kornaś S, Skalska M, Nowosad B, Gawor J, Kharchenko V, Cabaret J. Occurrence of strongyles (Strongylidae) in horses from small farms on the basis of necropsy. Pol J Vet Sci 12(2):225–230.
    pubmed: 19645353
  28. Kornaś S, Cabaret J, Skalska M, Nowosad B. Horse infection with intestinal helminths in relation to age, sex, access to grass and farm system. Vet Parasitol 174:285–291.
    pubmed: 20933334doi: 10.1016/j.vetpar.2010.09.007google scholar: lookup
  29. Kuzmina TA, Kharchenko VO. Anthelmintic resistance in cyathostomins of brood horses in Ukraine and influence of anthelmintic treatments on strongylid community structure. Vet Parasitol 154:277–288.
    pubmed: 18485600doi: 10.1016/j.vetpar.2008.03.024google scholar: lookup
  30. Kuzmina TA, Kharchenko VA, Starovir AI, Dvojnos GM. Analysis of the strongylid nematodes (Nematoda: Strongylidae) community after deworming of brood horses in Ukraine. Vet Parasitol 131:283–290.
    pubmed: 15979240doi: 10.1016/j.vetpar.2005.05.010google scholar: lookup
  31. Kuzmina TA, Kharchenko VA, Zvegintsova NS. Comparative study of the intestinal strongylid communities of equidae in the Askania-Nova biosphere reserve, Ukraine. Helminthol 44:62–69.
    doi: 10.2478/s11687-007-0005-9google scholar: lookup
  32. Kuzmina T, Kornaś S, Basiaga M, Kharchenko V, Vyniarska A. Biodiversity of strongylids (Nematoda: Strongylidae) communities in domestic horses from Poland and Ukraine. Helminthol 48:77–84.
    doi: 10.2478/s11687-011-0013-7google scholar: lookup
  33. Kuzmina TA, Lyons ET, Tolliver SC, Dzeverin II, Kharchenko VA. Fecundity of various species of strongylids (Nematoda: Strongylidae) – parasites of domestic horses. Parasitol Res 111:2265–2271.
    pubmed: 22903448doi: 10.1007/s00436-012-3077-5google scholar: lookup
  34. Kuzmina TA, Kharchenko VA, Zvegintsova NS, Zhang L, Liu J. Strongylids (Nematoda: Strongylidae) in two zebra species from the “Askania-Nova” biosphere reserve, Ukraine: biodiversity and parasite community structure. Helminthol 50:172–180.
    doi: 10.2478/s11687-013-0128-0google scholar: lookup
  35. 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 227:56–63.
    pubmed: 27523938doi: 10.1016/j.vetpar.2016.07.024google scholar: lookup
  36. Kuzmina TA, Zvegintsova NS, Yasynetska NI, Kharchenko VA. Anthelmintic resistance in strongylids (Nematoda: Strongylidae) parasitizing wild and domestic equids in the Askania Nova Biosphere Reserve, Ukraine. Ann Parasitol 66:49–60.
    pubmed: 32198995doi: 10.17420/ap6601.237google scholar: lookup
  37. Lichtenfels JR, Kharchenko VA, Dvojnos GM. Illustrated identification keys to strongylid parasites (strongylidae: Nematoda) of horses, zebras and asses (Equidae). Vet Parasitol 156:4–161.
    pubmed: 18603375doi: 10.1016/j.vetpar.2008.04.026google scholar: lookup
  38. Louro M, Kuzmina TA, Bredtmann CM, Diekmann I, de Carvalho LMM, von Samson-Himmelstjerna G, Krücken J. Genetic variability, cryptic species and phylogenetic relationship of six cyathostomin species based on mitochondrial and nuclear sequences. Sci Rep 11(1):8245.
    pmc: PMC8050097pubmed: 33859247doi: 10.1038/s41598-021-87500-8google scholar: lookup
  39. Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection. Vet Parasitol 85:113–122.
    pubmed: 10485358doi: 10.1016/s0304-4017(99)00092-8google scholar: lookup
  40. Lyons ET, Tolliver SC, Drudge JH, Stamper S, Swerczek TW, Granstrom DE. A study (1977–1992) of population dynamics of endoparasites featuring benzimidazole-resistant small strongyles (population S) in Shetland ponies. Vet Parasitol 66:75–86.
    pubmed: 8988558doi: 10.1016/s0304-4017(96)00998-3google scholar: lookup
  41. Lyons ET, Tolliver SC, Drudge JH. Historical perspective of cyathostomes: prevalence, treatment and control programs. Vet Parasitol 85:97–111.
    pubmed: 10485357doi: 10.1016/s0304-4017(99)00091-6google scholar: lookup
  42. Lyons ET, Tolliver SC, Collins SS, Drudge JH. Transmission of endoparasites in horse foals born on the same pasture on a farm in central Kentucky (1996–1999). Vet Parasitol 97:113–121.
    pubmed: 11358626doi: 10.1016/s0304-4017(01)00393-4google scholar: lookup
  43. Lyons ET, Bolin DC, Bryant UK, Cassone LM, Jackson CB, Janes JG, Kennedy LA, Loynachan AT, Boll KR, Burkhardt AS, Langlois EL, Minnis SM, Welsh SC, Scare JA. Postmortem examination (2016–2017) of weanling and older horses for the presence of select species of endoparasites: Gasterophilus spp., Anoplocephala spp. and Strongylus spp. in specific anatomical sites. Vet Parasitol Reg Stud Rep 13:98–104.
    pubmed: 31014896doi: 10.1016/j.vprsr.2018.01.004google scholar: lookup
  44. Matthews JB. An update on cyathostomins: anthelmintic resistance and worm control. Equine Vet Educ 20:552–560.
    doi: 10.2746/095777308x363912google scholar: lookup
  45. Matthews JB. Anthelmintic resistance in equine nematodes. Int J Parasitol Drugs Drug Resist 4:310–315.
    pmc: PMC4266799pubmed: 25516842doi: 10.1016/j.ijpddr.2014.10.003google scholar: lookup
  46. Matthews JB, Peczak N, Lightbody KL. The use of innovative diagnostics to inform sustainable control of equine helminth infections. Pathogens 12:1233.
    pmc: PMC10610145pubmed: 37887749doi: 10.3390/pathogens12101233google scholar: lookup
  47. Mfitilodze MW, Hutchinson GW. Prevalence and abundance of equine strongyles (Nematoda: Strongyloidea) in tropical Australia. J Parasitol 76:487–494.
    pubmed: 2380857
  48. Nielsen MK. Sustainable equine parasite control: perspectives and research needs. Vet Parasitol 185:32–44.
    pubmed: 22055611doi: 10.1016/j.vetpar.2011.10.012google scholar: lookup
  49. Nielsen MK. Anthelmintic resistance in equine nematodes: current status and emerging trends. Int J Parasitol Drugs Drug Resist 20:76–88.
    pmc: PMC9630620pubmed: 36342004doi: 10.1016/j.ijpddr.2022.10.005google scholar: lookup
  50. Nielsen MK, Reinemeyer CR. Handbook of equine parasite control, 2nd edn. .
    doi: 10.1002/9781119382829google scholar: lookup
  51. Nielsen MK, Baptiste KE, Tolliver SC, Collins SS, Lyons ET. Analysis of multiyear studies in horses in Kentucky to ascertain whether counts of eggs and larvae per gram of feces are reliable indicators of numbers of strongyles and ascarids present. Vet Parasitol 174:77–84.
    pubmed: 20850927doi: 10.1016/j.vetpar.2010.08.007google scholar: lookup
  52. Nielsen MK, Branan MA, Wiedenheft AM, Digianantonio R, Scare JA, Bellaw JL, Garber LP, Kopral CA, Phillippi-Taylor AM, Traub-Dargatz JL. Risk factors associated with strongylid egg count prevalence and abundance in the United States equine population. Vet Parasitol 257:58–68.
    pubmed: 29773232doi: 10.1016/j.vetpar.2018.05.006google scholar: lookup
  53. Nielsen MK, Gee EK, Hansen A, Waghorn T, Bell J, Leathwick DM. Monitoring equine ascarid and cyathostomin parasites: evaluating health parameters under different treatment regimens. Equine Vet J 53:902–910.
    pubmed: 33119179doi: 10.1111/evj.13374google scholar: lookup
  54. 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 52:787–798.
    pubmed: 36244428doi: 10.1016/j.ijpara.2022.09.003google scholar: lookup
  55. Nielsen MK, Slusarewicz P, Kuzmina TA, Denwood MJ. US-wide equine strongylid egg count data demonstrate seasonal and regional trends. Parasitol 17:1–8.
    pmc: PMC11428020pubmed: 38629125doi: 10.1017/s0031182024000489google scholar: lookup
  56. Nielsen MK, MittelL., Grice A, Erskine M, Graves E, Vaala W, Tully RC, French DD, Bowman R, Kaplan RM. AAEP parasite control guidelines. American Association of Equine Practitioners .
  57. Ogbourne CP. Pathogenesis of cyathostome (Trichonema) infections of the horse. A review. Misc Publ Comm Inst Helminthol 5:1–25.
  58. Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Solymos P, Stevens MHH, Szoecs E, Wagner H, Barbour M, Bedward M, Bolker B, Borcard D, Carvalho G, Chirico M, De Caceres M, Durand S, Evangelista HBA, FitzJohn R, Friendly M, Furneaux B, Hannigan G, Hill MO, Lahti L, McGlinn D, Ouellette M., Ribeiro Cunha E, Smith T, Stier A, Ter Braak CJF, Weedon J. vegan: community ecology package (Version 2.6–4) [R package]. CRAN .
  59. Osterman Lind E, Höglund J, Ljungström BL, Nilsson O, Uggla A. A field survey on the distribution of strongyle infections of horses in Sweden and factors affecting faecal egg counts. Equine Vet J 31:68–72.
    pubmed: 9952332
  60. Osterman Lind E, Eysker M, Nilsson O, Uggla A, Höglund J. Expulsion of small strongyle nematodes (Cyathostomin spp.) following deworming of horses on a stud farm in Sweden. Vet Parasitol 115:289–299.
    pubmed: 12944042doi: 10.1016/s0304-4017(03)00200-0google scholar: lookup
  61. Osterman Lind E, 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 Comm 31:53–65.
    pubmed: 17186406doi: 10.1007/s11259-006-3402-5google scholar: lookup
  62. Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter?. Vet Parasitol 201:1–8.
    pubmed: 24485565doi: 10.1016/j.vetpar.2014.01.004google scholar: lookup
  63. Pfister K, van Doorn D. New perspectives in equine intestinal parasitic disease: insights in monitoring helminth infections. Vet Clin North Am Equine Pract 34:141–153.
    pubmed: 29426708doi: 10.1016/j.cveq.2017.11.009google scholar: lookup
  64. Pilo C, Altea A, Pirino S, Nicolussi P, Varcasia A, Genchi M, Scala A. Strongylus vulgaris (Looss, 1900) in horses in Italy: is it still a problem?. Vet Parasitol 184:161–167.
    pubmed: 21962966doi: 10.1016/j.vetpar.2011.09.016google scholar: lookup
  65. Poissant J, Gavriliuc S, Bellaw J, Redman EM, Avramenko RW, Robinson D, Workentine ML, Shury TK, Jenkins EJ, McLoughlin PD, Nielsen MK, Gilleard JS. A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses. Int J Parasitol 51:183–192.
    pubmed: 33242465doi: 10.1016/j.ijpara.2020.09.003google scholar: lookup
  66. R Core Team. R: a language and environment for statistical computing (Version 2023) [Software]. R Foundation for Statistical Computing .
  67. Reiczigel J, Abonyi-Tóth Z, Singer J. An exact confidence set for two binomial proportions and exact unconditional confidence intervals for the difference and ratio of proportions. Comput Stat Data Anal 52:5046–5053.
    doi: 10.1016/j.csda.2008.04.032google scholar: lookup
  68. Reinemeyer CR, Smith SA, Gabel AA, Herd RP. The prevalence and intensity of internal parasites of horses in the U.S.A.. Vet Parasitol 15:75–83.
    pubmed: 6237483
  69. Relf VE, Morgan ER, Hodgkinson JE, Matthews JB. Helminth egg excretion with regard to age, gender and management practices on UK thoroughbred studs. Parasitol 140:641–652.
    pubmed: 23351718doi: 10.1017/s0031182012001941google scholar: lookup
  70. Rózsa L, Reiczigel J, Majoros G. Quantifying parasites in samples of hosts. J Parasitol 86:228–232.
    pubmed: 10780537doi: 10.1645/0022-3395(2000)086[0228:qpisoh]2.0.co;2google scholar: lookup
  71. Saeed K, Qadir Z, Ashraf K, Ahmad N. Role of intrinsic and extrinsic epidemiological factors on strongylosis in horses. J Anim Plant Sci 20:277–280.
  72. Sallé G, Kornaś S, Basiaga M. Equine strongyle communities are constrained by horse sex and species dipersal-fecundity trade-off. Parasit Vectors 11:279.
    pmc: PMC5930759pubmed: 29716644doi: 10.1186/s13071-018-2858-9google scholar: lookup
  73. Sallé G, Guillot J, Tapprest J, Foucher N, Sevin C, Laugier C. Compilation of 29 years of postmortem examinations identifies major shifts in equine parasite prevalence from 2000 onwards. Int J Parasitol 50:125–132.
    pubmed: 31981673doi: 10.1016/j.ijpara.2019.11.004google scholar: lookup
  74. 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 52:763–774.
    pubmed: 36208676doi: 10.1016/j.ijpara.2022.08.002google scholar: lookup
  75. Silva AM, Costa HMA, Santos HA, Carvalho RO. Cyathostominae (Nematoda) parasites of Equus caballus some Brazilian states. Vet Parasitol 86:15–21.
    pubmed: 10489198doi: 10.1016/s0304-4017(99)00078-3google scholar: lookup
  76. Slivinska K, Kharchenko V, Wróblewski Z, Gawor J, Kuzmina T. Parasitological survey of Polish primitive horses (Equus caballus gmelini Ant.): influence of age, sex and management strategies on the parasite community. Helminthol 53:233–242.
    doi: 10.1515/helmin-2016-0023google scholar: lookup
  77. Studzińska MB, Tomczuk K, Demkowska-Kutrzepa M, Szczepaniak K. The Strongylidae belonging to Strongylus genus in horses from southeastern Poland. Parasitol Res 111:1417–1421.
    pmc: PMC3447134pubmed: 22961235doi: 10.1007/s00436-012-3087-3google scholar: lookup
  78. Tolliver SC, Lyons ET, Drudge JH, Stamper S, Granstrom DE. Critical tests of thiabendazole, oxibendazole, and oxfendazole for drug resistance of population-B equine small strongyles (1989 and 1990). Am J Vet Res 54:908–913.
    pubmed: 8323061
  79. Traversa D, Kuzmina T, Kharchenko VA, Iorio R, Klei TR, Otranto D. Haplotypic variability within the mitochondrial gene encoding for the cytochrome c oxidase 1 (cox1) of Cylicocyclus nassatus (Nematoda, Strongylida): evidence for an affiliation between parasitic populations and domestic and wild equid hosts. Vet Parasitol 156:241–247.
    pubmed: 18619736doi: 10.1016/j.vetpar.2008.05.031google scholar: lookup
  80. 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 206:246–252.
    pubmed: 25458565doi: 10.1016/j.vetpar.2014.10.004google scholar: lookup
  81. Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen TL, Miller E, Bache SM, Müller K, Ooms J, Robinson D, Seidel DP, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H. Welcome to the tidyverse. J Open Source Softw 4(43):1686.
    doi: 10.21105/joss.01686google scholar: lookup
  82. Wood EL, Matthews JB, Stephenson S, Slote M, Nussey DH. Variation in fecal egg counts in horses managed for conservation purposes: individual egg shedding consistency, age effects and seasonal variation. Parasitol 140:115–128.
    pubmed: 22894917doi: 10.1017/s003118201200128xgoogle scholar: lookup

Citations

This article has been cited 1 times.
  1. Fonseca JDS, Barbosa BB, Silva AP, Vázquez MSA, Cazapal Monteiro CF, Santos HA, de Araújo JV. Using Biocontrol Fungi to Control Helminthosis in Wild Animals: An Innovative Proposal for the Health and Conservation of Species. Pathogens 2025 Aug 5;14(8).
    doi: 10.3390/pathogens14080775pubmed: 40872285google scholar: lookup
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