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Frontiers in veterinary science2022; 9; 892920; doi: 10.3389/fvets.2022.892920

Occurrence of Strongylid Nematode Parasites on Horse Farms in Berlin and Brandenburg, Germany, With High Seroprevalence of Strongylus vulgaris Infection.

Abstract: The infection of horses with strongylid nematodes is highly prevalent, with multi-species infections being the rule. spp. and in particular are amongst the most pathogenic strongyle equine parasites. Presumably due to regular strategic anthelmintic treatments in combination with long prepatencies, prevalence of these worms was severely reduced in past decades. In this study, 484 horses from 48 farms in Berlin/Brandenburg, Germany were sampled between May 2017 and January 2018. Mini-FLOTAC and combined sedimentation/flotation were used to analyse faecal samples and larval cultures were carried out from individual strongyle infected horses for molecular testing for spp. infection. Additionally, for , antibodies against a recombinant larval antigen were quantified in an ELISA. Strongyle type eggs were detected in 66.7% of the individual faecal samples. Nematode DNA was amplifiable from 311 samples and and were detected in four (1.3%) and 10 (6.3%) of these, respectively, the latter using a novel high-resolution-melt PCR targeting , and . On the farm level, prevalence for spp. by PCR was 12.5%. Applying a conservative cut-off (sensitivity 0.43, specificity 0.96), 21.2% of all serum samples were positive for antibodies against larvae (83.3% prevalence on farm level). Newly developed pyrosequencing assays to analyse putatively benzimidazole resistance associated polymorphisms in codons 167, 198, and 200 of the isotype 1 β-tubulin gene of did not detect such polymorphisms in the four positive samples. Low age and increasing access to pasture were risk factors for egg shedding and seropositivity for . Time since last treatment increased whereas use of moxidectin and ivermectin for the last treatment decreased the risk for strongyle egg shedding. Noteworthy, horses under selective treatment had significantly higher odds to be seropositive for anti- antibodies than horses treated four times per year (odds ratio 4.4). The serological findings suggest that exposure to is considerably higher than expected from direct diagnostic approaches. One potential explanation is the contamination of the environment by a few infected horses, leading to the infection of many horses with larvae that never reach maturity due to regular anthelmintic treatments.
Publication Date: 2022-06-10 PubMed ID: 35754549PubMed Central: PMC9226773DOI: 10.3389/fvets.2022.892920Google Scholar: Lookup
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  • Journal Article

Summary

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The research paper explores the prevalence of strongylid nematodes, particularly Strongylus vulgaris, in horses across 48 farms in Berlin and Brandenburg, Germany. It suggests that the infection is more rampant than anticipated due to environmental contamination caused by a few infected horses despite regular anthelmintic treatments.

Research Methodology used in the study

  • The authors of the study collected samples from 484 horses across 48 different farms situated in Berlin and Brandenburg, Germany, from May 2017 to January 2018.
  • Two different techniques, namely Mini-FLOTAC and combined sedimentation/flotation, were employed for analysing individual faecal samples. The presence of strongyle eggs was indicative of an infection.
  • Larval cultures obtained from these horses were subjected to molecular testing for Strongylus spp. infection.
  • In addition, for Strongylus vulgaris, antibodies against a recombinant larval antigen were quantified using an Enzyme-linked immunosorbent assay (ELISA).

Study Findings

  • The study found strongyle type eggs in 66.7% individual faecal samples. Moreover, nematode DNA was obtained from 311 samples with Strongylus vulgaris and Strongylus spp. found in 1.3% and 6.3% of these samples, respectively.
  • The farm-level prevalence was estimated to be 12.5% for Strongylus spp.
  • With defined sensitivity and specificity values, 21.2% of serum samples showed positivity for antibodies against Strongylus vulgaris larvae.
  • Younger horses and those with increased access to pasture were identified as high-risk groups for strongyle infection.

Inference and Implications

  • The inference drawn from the study indicated a much higher than anticipated exposure to Strongylus vulgaris from direct diagnostic approaches.
  • The higher exposure rates could likely be due to environmental contamination from a few infected horses, culminating in the mass infection of horses with larvae.
  • The researchers noticed such high infection rates despite the regular usage of anthelmintic treatments, suggesting that these treatments might not be entirely effective in controlling the prevalence of the parasites.

Odds associated with Treatment Regimes

  • The study also noted that the time elapsed since the last administered treatment resulted in a higher probability of Strongylus egg shedding.
  • The use of anthelmintic drugs such as moxidectin and ivermectin in the last treatment considerably lowered the risk of egg shedding.
  • However, horses treated only selectively demonstrated significantly higher odds (odds ratio 4.4) of being seropositive than those treated four times a year.

Cite This Article

APA
Jürgenschellert L, Krücken J, Bousquet E, Bartz J, Heyer N, Nielsen MK, von Samson-Himmelstjerna G. (2022). 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. https://doi.org/10.3389/fvets.2022.892920

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 892920
PII: 892920

Researcher Affiliations

Jürgenschellert, Laura
  • Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.
Krücken, Jürgen
  • Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.
Bousquet, Eric
  • Virbac, Carros, France.
Bartz, Jürgen
  • Virbac Tierazneimittel GmbH, Bad Oldesloe, Germany.
Heyer, Nina
  • Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.
Nielsen, Martin K
  • M.H. Gluck Equine Research Center, University of Kentucky, Lexington, KY, United States.
von Samson-Himmelstjerna, Georg
  • Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.

Conflict of Interest Statement

JB is employed by Virbac Tierarzneimittel GMBH and EB by Virbac France. GS-H declares that he has repeatedly acted as consultant for veterinary pharmaceutical and diagnostic companies and has previous and ongoing research collaborations with various companies. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 106 references
  1. Lichtenfels JR, Kharchenko VA, Dvojnos GM. Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae).. Vet Parasitol 2008 Sep 15;156(1-2):4-161.
    doi: 10.1016/j.vetpar.2008.04.026pubmed: 18603375google scholar: lookup
  2. Corning S. Equine cyathostomins: a review of biology, clinical significance and therapy.. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S1.
    doi: 10.1186/1756-3305-2-S2-S1pmc: PMC2751837pubmed: 19778462google scholar: lookup
  3. Matthews J. An update on cyathostomins: anthelmintic resistance and worm control.. Equine Vet Educ (2008) 20:552–60.
    doi: 10.2746/095777308X363912pubmed: 0google scholar: lookup
  4. Kaplan RM. Anthelmintic resistance in nematodes of horses.. Vet Res 2002 Sep-Oct;33(5):491-507.
    doi: 10.1051/vetres:2002035pubmed: 12387486google scholar: lookup
  5. Kuz'mina TA. [Strongylids (Nematoda: Strongylidae) of domestic horses in Ukraine: modern state of Fauna and structure of the parasite community].. Parazitologiia 2012 Mar-Apr;46(2):127-38.
    pubmed: 22834350
  6. Chapman MR, French DD, Taylor HW, Klei TR. One season of pasture exposure fails to induce a protective resistance to cyathostomes but increases numbers of hypobiotic third-stage larvae.. J Parasitol 2002 Aug;88(4):678-83.
    doi: 10.1645/0022-3395(pubmed: 12197113google scholar: lookup
  7. Eysker M, Boersema JH, Kooyman FN. Seasonally inhibited development of cyathostomine nematodes in Shetland ponies in The Netherlands.. Vet Parasitol 1990 Jul;36(3-4):259-64.
    doi: 10.1016/0304-4017(90)90037-Cpubmed: 2399646google scholar: lookup
  8. Eysker M, Mirck MH. The distribution of inhibited early third stage Cyathostominae larvae in the large intestine of the horse.. Z Parasitenkd 1986;72(6):815-20.
    doi: 10.1007/BF00925101pubmed: 3799011google scholar: lookup
  9. Andersen UV, Howe DK, Olsen SN, Nielsen MK. Recent advances in diagnosing pathogenic equine gastrointestinal helminths: the challenge of prepatent detection.. Vet Parasitol 2013 Feb 18;192(1-3):1-9.
    doi: 10.1016/j.vetpar.2012.11.003pubmed: 23199789google scholar: lookup
  10. Pfister K, van Doorn D. New Perspectives in Equine Intestinal Parasitic Disease: Insights in Monitoring Helminth Infections.. Vet Clin North Am Equine Pract 2018 Apr;34(1):141-153.
    doi: 10.1016/j.cveq.2017.11.009pubmed: 29426708google scholar: lookup
  11. Wirtherle N, Schnieder T, von Samson-Himmelstjerna G. Prevalence of benzimidazole resistance on horse farms in Germany.. Vet Rec 2004 Jan 10;154(2):39-41.
    doi: 10.1136/vr.154.2.39pubmed: 14758828google scholar: lookup
  12. Fritzen B, Rohn K, Schnieder T, von Samson-Himmelstjerna G. Endoparasite control management on horse farms--lessons from worm prevalence and questionnaire data.. Equine Vet J 2010 Jan;42(1):79-83.
    doi: 10.2746/042516409X471485pubmed: 20121919google scholar: lookup
  13. 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 2011 May;108(5):1083-91.
    doi: 10.1007/s00436-011-2362-zpubmed: 21472400google scholar: lookup
  14. Kaspar A, Pfister K, Nielsen MK, Silaghi C, Fink H, Scheuerle MC. Detection of Strongylus vulgaris in equine faecal samples by real-time PCR and larval culture - method comparison and occurrence assessment.. BMC Vet Res 2017 Jan 11;13(1):19.
    doi: 10.1186/s12917-016-0918-ypmc: PMC5225560pubmed: 28077153google scholar: lookup
  15. Schneider S, Pfister K, Becher AM, Scheuerle MC. Strongyle infections and parasitic control strategies in German horses - a risk assessment.. BMC Vet Res 2014 Nov 12;10:262.
    doi: 10.1186/s12917-014-0262-zpmc: PMC4232665pubmed: 25387542google scholar: lookup
  16. Monahan CM, Chapman MR, Taylor HW, French DD, Klei TR. Comparison of moxidectin oral gel and ivermectin oral paste against a spectrum of internal parasites of ponies with special attention to encysted cyathostome larvae.. Vet Parasitol 1996 Jun;63(3-4):225-35.
    doi: 10.1016/0304-4017(95)00910-8pubmed: 8966989google scholar: lookup
  17. Klei TR, Turk MA, McClure JR, Holmes RA, Dennis VA, Chapman MR. Effects of repeated Strongylus vulgaris inoculations and concurrent ivermectin treatments on mesenteric arterial lesions in pony foals.. Am J Vet Res 1990 Apr;51(4):654-60.
    pubmed: 2327628
  18. Greite L. Untersuchungen Zur Verbreitung Von Strongylus vulgaris Im Rahmen der selektiven Entwurmung Bei Pferden in Süddeutschland. Dissertation Ludwig-Maximilians-Universität, München, Germany; (2013).
  19. Beelitz P, Göbel E, Gothe R. [Spectrum of species and incidence of endoparasites in foals and their mother mares from breeding farms with and without anthelmintic prophylaxis in upper Bavaria].. Tierarztl Prax 1996 Feb;24(1):48-54.
    doi: 10.1515/9783486787122.48pubmed: 8720956google scholar: lookup
  20. Beelitz P, Göbel E, Gothe R. Endoparasiten von Eseln und Pferden bei gemeinsamer Haltung in Oberbayern: Artenspektrum und Befallshäufigkeit.. Tierartzl Praxis (1996) 24:471–5.
  21. Cirak VY, Hermosilla C, Bauer C. Study on the gastrointestinal parasite fauna of ponies in northern Germany.. Appl Parasitol 1996 Dec;37(4):239-44.
    pubmed: 9060170
  22. Kiedrowski C. Helminthologische Untersuchungen an Pferden vor und nach der Schlachtung. Dissertation Freie Universität Berlin, Berlin, Germany; (1959).
  23. Fritzen BM. Untersuchungen Zum Vorkommen Von Anthelminthika-Resistenz in Nordrhein-Westfälischen Pferdebeständen. Dissertation Institute for Parsitology, University of Veterinary Medicine, Hannover, Germany DVG-Service; (2005).
  24. Duncan JL, Pirie HM. The life cycle of Strongylus vulgaris in the horse.. Res Vet Sci 1972 Jul;13(4):374-9.
    doi: 10.1016/S0034-5288(18)34017-7pubmed: 5072578google scholar: lookup
  25. ENIGK K. [Further studies on the biology of Strongylus vulgaris (Nematodes) in the host].. Z Tropenmed Parasitol 1951 Apr;2(4):523-35.
    pubmed: 14837165
  26. Duncan JL, Campbell JR. Further observations on the maintenance of a monospecific infection of Strongylus vulgaris in the horse.. Vet Rec 1973 May 19;92(20):533.
    doi: 10.1136/vr.92.20.533-apubmed: 4721941google scholar: lookup
  27. Pihl TH, Nielsen MK, Olsen SN, Leifsson PS, Jacobsen S. Nonstrangulating intestinal infarctions associated with Strongylus vulgaris: Clinical presentation and treatment outcomes of 30 horses (2008-2016).. Equine Vet J 2018 Jul;50(4):474-480.
    doi: 10.1111/evj.12779pubmed: 29112788google scholar: lookup
  28. Duncan JL, Pirie HM. The pathogenesis of single experimental infections with Strongylus vulgaris in foals.. Res Vet Sci 1975 Jan;18(1):82-93.
    doi: 10.1016/S0034-5288(18)33635-Xpubmed: 1118668google scholar: lookup
  29. Bollinger O. Die Kolik der Pferde und das Wurmaneurysma der Eingeweidearterien.. Münchener Sitzungsberichte Königliche Bayerischen Akademie der Wissenschaften Mathematisch-naturwissenschaftliche Abteilung (1870).
  30. Olt A. Das Aneurysma Verminosum des Pferdes und seine unbekannten Beziehungen zur Kolik.. Dtsch Tierarztl Wschr (1932) 40:326–32.
  31. van Andel AC, Gruys E, Kroneman J, Veerkamp J. Amyloid in the horse: a report of nine cases.. Equine Vet J 1988 Jul;20(4):277-85.
  32. Greatorex JC. Diagnosis and treatment of "verminous aneurysm" formation in the horse.. Vet Rec 1977 Sep 3;101(10):184-7.
    doi: 10.1136/vr.101.10.184pubmed: 579006google scholar: lookup
  33. Drudge JH, Lyons ET. Large strongyles. Recent advances.. Vet Clin North Am Equine Pract 1986 Aug;2(2):263-80.
    doi: 10.1016/S0749-0739(17)30716-2pubmed: 3527373google scholar: lookup
  34. Pauli B, Althaus S, Von Tscharner C. [Arterial repair after mechanical injury by migrating fourth-stage larvae of Strongylus vulgaris in the horse (a light and electron microscopic study) (author's transl)].. Beitr Pathol 1975 Aug;155(4):357-78.
    doi: 10.1016/S0005-8165(75)80101-6pubmed: 1180809google scholar: lookup
  35. Nielsen MK, Jacobsen S, Olsen SN, Bousquet E, Pihl T. Nonstrangulating intestinal infarction associated with Strongylus vulgaris in referred Danish equine cases.. Equine Vet J 2016 May;48(3):376-9.
    doi: 10.1111/evj.12422pubmed: 25604521google scholar: lookup
  36. McCraw BM, Slocombe JO. Strongylus edentatus: development and lesions from ten weeks postinfection to patency.. Can J Comp Med 1978 Jul;42(3):340-56.
    pmc: PMC1277649pubmed: 688075
  37. McCraw BM, Slocombe JO. Early development of and pathology associated with Strongylus edentatus.. Can J Comp Med 1974 Apr;38(2):124-38.
    pmc: PMC1319985pubmed: 4274818
  38. McCraw BM, Slocombe JO. Strongylus equinus: development and pathological effects in the equine host.. Can J Comp Med 1985 Oct;49(4):372-83.
    pmc: PMC1236195pubmed: 4075237
  39. Malan FS, De Vos V, Reinecke RK, Pletcher JM. Studies on Strongylus asini. I. Experimental infestation of equines.. Onderstepoort J Vet Res 1982 Sep;49(3):151-4.
    pubmed: 7177594
  40. Round MC. The prepatent period of some horse nematodes determined by experimental infection.. J Helminthol 1969;43(1):185-92.
    doi: 10.1017/S0022149X00004016pubmed: 5381124google scholar: lookup
  41. Love S, Duncan JL. The development of naturally acquired cyathostome infection in ponies.. Vet Parasitol 1992 Sep;44(1-2):127-42.
    doi: 10.1016/0304-4017(92)90151-Xpubmed: 1441184google scholar: lookup
  42. Reinemeyer CR, Herd RP, Gabel AA. Distribution of adult and larval cyathostomes in helminth-naive foals after primary infection.. Equine Vet J 1988 Jul;20(4):296-7.
  43. Murphy D, Love S. The pathogenic effects of experimental cyathostome infections in ponies.. Vet Parasitol 1997 Jun;70(1-3):99-110.
    doi: 10.1016/S0304-4017(96)01153-3pubmed: 9195714google scholar: lookup
  44. Gibson T. The effect of repeated anthelmintic treatment with phenothiazine on the faecal egg counts of housed horses, with some observations on the life cycle of Trichonema Spp. in the horse.. J Helminthol (1953) 27:29–40.
    doi: 10.1017/S0022149X00023488google scholar: lookup
  45. Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection.. Vet Parasitol 1999 Aug 31;85(2-3):113-21; discussion 121-2, 215-25.
    doi: 10.1016/S0304-4017(99)00092-8pubmed: 10485358google scholar: lookup
  46. Giles CJ, Urquhart KA, Longstaffe JA. Larval cyathostomiasis (immature trichonema-induced enteropathy): a report of 15 clinical cases.. Equine Vet J 1985 May;17(3):196-201.
  47. RUSSELL AF. The development of helminthiasis in thoroughbred foals.. J Comp Pathol Ther 1948 Apr;58(2):107-27.
    doi: 10.1016/S0368-1742(48)80009-3pubmed: 18861669google scholar: lookup
  48. Nielsen MK, Peterson DS, Monrad J, Thamsborg SM, Olsen SN, Kaplan RM. Detection and semi-quantification of Strongylus vulgaris DNA in equine faeces by real-time quantitative PCR.. Int J Parasitol 2008 Mar;38(3-4):443-53.
    doi: 10.1016/j.ijpara.2007.07.014pubmed: 17889881google scholar: lookup
  49. Campbell AJ, Gasser RB, Chilton NB. Differences in a ribosomal DNA sequence of Strongylus species allows identification of single eggs.. Int J Parasitol 1995 Mar;25(3):359-65.
    doi: 10.1016/0020-7519(94)00116-6pubmed: 7601594google scholar: lookup
  50. Gasser RB, Stevenson LA, Chilton NB, Nansen P, Bucknell DG, Beveridge I. Species markers for equine strongyles detected in intergenic rDNA by PCR-RFLP.. Mol Cell Probes 1996 Oct;10(5):371-8.
    doi: 10.1006/mcpr.1996.0050pubmed: 8910892google scholar: lookup
  51. Hung GC, Gasser RB, Beveridge I, Chilton NB. Species-specific amplification by PCR of ribosomal DNA from some equine strongyles.. Parasitology 1999 Jul;119 ( Pt 1):69-80.
    doi: 10.1017/S0031182099004497pubmed: 10446706google scholar: lookup
  52. Bracken MK, Wøhlk CB, Petersen SL, Nielsen MK. Evaluation of conventional PCR for detection of Strongylus vulgaris on horse farms.. Vet Parasitol 2012 Mar 23;184(2-4):387-91.
    doi: 10.1016/j.vetpar.2011.08.015pubmed: 21889849google scholar: lookup
  53. Tzelos T, Geyer KK, Mitchell MC, McWilliam HEG, Kharchenko VO, Burgess STG, Matthews JB. Characterisation of serum IgG(T) responses to potential diagnostic antigens for equine cyathostominosis.. Int J Parasitol 2020 Apr;50(4):289-298.
    doi: 10.1016/j.ijpara.2020.01.004pubmed: 32171845google scholar: lookup
  54. Andersen UV, Howe DK, Dangoudoubiyam S, Toft N, Reinemeyer CR, Lyons ET, Olsen SN, Monrad J, Nejsum P, Nielsen MK. SvSXP: a Strongylus vulgaris antigen with potential for prepatent diagnosis.. Parasit Vectors 2013 Apr 4;6:84.
    doi: 10.1186/1756-3305-6-84pmc: PMC3623896pubmed: 23557195google scholar: lookup
  55. 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 Nov 30;214(1-2):100-7.
    doi: 10.1016/j.vetpar.2015.10.003pubmed: 26477278google scholar: lookup
  56. Duncan JL, Bairden K, Abbott EM. Elimination of mucosal cyathostome larvae by five daily treatments with fenbendazole.. Vet Rec 1998 Mar 14;142(11):268-71.
    doi: 10.1136/vr.142.11.268pubmed: 9569480google scholar: lookup
  57. Matthews JB. Anthelmintic resistance in equine nematodes.. Int J Parasitol Drugs Drug Resist 2014 Dec;4(3):310-5.
  58. Nielsen MK, Reinemeyer CR, Donecker JM, Leathwick DM, Marchiondo AA, Kaplan RM. Anthelmintic resistance in equine parasites--current evidence and knowledge gaps.. Vet Parasitol 2014 Jul 30;204(1-2):55-63.
    doi: 10.1016/j.vetpar.2013.11.030pubmed: 24433852google scholar: lookup
  59. von Samson-Himmelstjerna G. Anthelmintic resistance in equine parasites - detection, potential clinical relevance and implications for control.. Vet Parasitol 2012 Apr 19;185(1):2-8.
    doi: 10.1016/j.vetpar.2011.10.010pubmed: 22100141google scholar: lookup
  60. Kaplan RM, Klei TR, Lyons ET, Lester G, Courtney CH, French DD, Tolliver SC, Vidyashankar AN, Zhao Y. Prevalence of anthelmintic resistant cyathostomes on horse farms.. J Am Vet Med Assoc 2004 Sep 15;225(6):903-10.
    doi: 10.2460/javma.2004.225.903pubmed: 15485051google scholar: lookup
  61. 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 Sep 10;188(3-4):294-300.
    doi: 10.1016/j.vetpar.2012.03.048pubmed: 22538094google scholar: lookup
  62. Saes IL, Vera JHS, Fachiolli DF, Yamada PH, Dellaqua JVT, Saes RL, Amarante AFT, Soutello RVG. Time required by different anthelmintics to reach expected efficacy levels in horses infected by strongyles.. Vet Parasitol 2016 Oct 15;229:90-92.
    doi: 10.1016/j.vetpar.2016.10.002pubmed: 27809986google scholar: lookup
  63. Lind EO, Kuzmina T, Uggla A, Waller PJ, Höglund J. A field study on the effect of some anthelmintics on cyathostomins of horses in sweden.. Vet Res Commun 2007 Jan;31(1):53-65.
    doi: 10.1007/s11259-006-3402-5pubmed: 17186406google scholar: lookup
  64. Traversa D, von Samson-Himmelstjerna G, Demeler J, Milillo P, Schürmann S, Barnes H, Otranto D, Perrucci S, di Regalbono AF, Beraldo P, Boeckh A, Cobb R. Anthelmintic resistance in cyathostomin populations from horse yards in Italy, United Kingdom and Germany.. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S2.
    doi: 10.1186/1756-3305-2-S2-S2pmc: PMC2751838pubmed: 19778463google scholar: lookup
  65. Vera JHS, Fachiolli DF, Ramires LM, de Lima Saes I, Yamada PH, Gonçalves JA, de Oliveira K, do Amarante AFT, de Soutello RVG. Eficacy of ivermectin, moxidectin and febendazole in equine in Brazil.. Vet Parasitol Reg Stud Reports 2020 Apr;20:100374.
    doi: 10.1016/j.vprsr.2020.100374pubmed: 32448518google scholar: lookup
  66. Nielsen MK, Branan MA, Wiedenheft AM, Digianantonio R, Scare JA, Bellaw JL, Garber LP, Kopral CA, Phillippi-Taylor AM, Traub-Dargatz JL. Anthelmintic efficacy against equine strongyles in the United States.. Vet Parasitol 2018 Aug 15;259:53-60.
    doi: 10.1016/j.vetpar.2018.07.003pubmed: 30056984google scholar: lookup
  67. Coles GC, Jackson F, Pomroy WE, Prichard RK, von Samson-Himmelstjerna G, Silvestre A, Taylor MA, Vercruysse J. The detection of anthelmintic resistance in nematodes of veterinary importance.. Vet Parasitol 2006 Mar 31;136(3-4):167-85.
    doi: 10.1016/j.vetpar.2005.11.019pubmed: 16427201google scholar: lookup
  68. Sangster NC, Prichard RK, Lacey E. Tubulin and benzimidazole-resistance in Trichostrongylus colubriformis (Nematoda).. J Parasitol 1985 Oct;71(5):645-51.
    doi: 10.2307/3281438pubmed: 3840531google scholar: lookup
  69. Gokbulut C, McKellar QA. Anthelmintic drugs used in equine species.. Vet Parasitol 2018 Sep 15;261:27-52.
    doi: 10.1016/j.vetpar.2018.08.002pubmed: 30253849google scholar: lookup
  70. Lacey E. The role of the cytoskeletal protein, tubulin, in the mode of action and mechanism of drug resistance to benzimidazoles.. Int J Parasitol 1988 Nov;18(7):885-936.
    doi: 10.1016/0020-7519(88)90175-0pubmed: 3066771google scholar: lookup
  71. Prichard R. Genetic variability following selection of Haemonchus contortus with anthelmintics.. Trends Parasitol 2001 Sep;17(9):445-53.
    doi: 10.1016/S1471-4922(01)01983-3pubmed: 11530357google scholar: lookup
  72. Kwa MS, Veenstra JG, Roos MH. Molecular characterisation of beta-tubulin genes present in benzimidazole-resistant populations of Haemonchus contortus.. Mol Biochem Parasitol 1993 Jul;60(1):133-43.
    doi: 10.1016/0166-6851(93)90036-Wpubmed: 8366887google scholar: lookup
  73. Ghisi M, Kaminsky R, Mäser P. Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes.. Vet Parasitol 2007 Mar 31;144(3-4):313-20.
    doi: 10.1016/j.vetpar.2006.10.003pubmed: 17101226google scholar: lookup
  74. Mohammedsalih KM, Krücken J, Bashar A, Juma FR, Abdalmalaik AAH, Khalafalla A, Abakar A, Coles G, von Samson-Himmelstjerna G. Susceptible trichostrongyloid species mask presence of benzimidazole-resistant Haemonchus contortus in cattle.. Parasit Vectors 2021 Feb 8;14(1):101.
    doi: 10.1186/s13071-021-04593-wpmc: PMC7869217pubmed: 33557939google scholar: lookup
  75. Martínez-Valladares M, Valderas-García E, Gandasegui J, Skuce P, Morrison A, Castilla Gómez de Agüero V, Cambra-Pellejà M, Balaña-Fouce R, Rojo-Vázquez FA. Teladorsagia circumcincta beta tubulin: the presence of the E198L polymorphism on its own is associated with benzimidazole resistance.. Parasit Vectors 2020 Sep 7;13(1):453.
    doi: 10.1186/s13071-020-04320-xpmc: PMC7487696pubmed: 32894163google scholar: lookup
  76. Dilks CM, Hahnel SR, Sheng Q, Long L, McGrath PT, Andersen EC. Quantitative benzimidazole resistance and fitness effects of parasitic nematode beta-tubulin alleles.. Int J Parasitol Drugs Drug Resist 2020 Dec;14:28-36.
  77. Redman E, Whitelaw F, Tait A, Burgess C, Bartley Y, Skuce PJ, Jackson F, Gilleard JS. The emergence of resistance to the benzimidazole anthlemintics in parasitic nematodes of livestock is characterised by multiple independent hard and soft selective sweeps.. PLoS Negl Trop Dis 2015 Feb;9(2):e0003494.
  78. Dilks CM, Koury EJ, Buchanan CM, Andersen EC. Newly identified parasitic nematode beta-tubulin alleles confer resistance to benzimidazoles.. Int J Parasitol Drugs Drug Resist 2021 Dec;17:168-175.
  79. Blackhall WJ, Kuzmina T, von Samson-Himmelstjerna G. β-Tubulin genotypes in six species of cyathostomins from anthelmintic-naive Przewalski and benzimidazole-resistant brood horses in Ukraine.. Parasitol Res 2011 Oct;109(4):1199-203.
    doi: 10.1007/s00436-011-2426-0pubmed: 21553015google scholar: lookup
  80. Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter?. Vet Parasitol 2014 Mar 17;201(1-2):1-8.
    doi: 10.1016/j.vetpar.2014.01.004pubmed: 24485565google scholar: lookup
  81. Becher AM, van Doorn DC, Pfister K, Kaplan RM, Reist M, Nielsen MK. Equine parasite control and the role of national legislation - A multinational questionnaire survey.. Vet Parasitol 2018 Aug 15;259:6-12.
    doi: 10.1016/j.vetpar.2018.07.001pubmed: 30056985google scholar: lookup
  82. Tydén E, Enemark HL, Franko MA, Höglund J, Osterman-Lind E. Prevalence of Strongylus vulgaris in horses after ten years of prescription usage of anthelmintics in Sweden.. Vet Parasitol X 2019 Nov;2:100013.
    doi: 10.1016/j.vpoa.2019.100013pmc: PMC7458386pubmed: 32904767google scholar: lookup
  83. Cain JL, Jarisch K, Macaluso KR, Luedtke BE. Correlation between fecal egg count, presence of Strongylus vulgaris, and body score of feral horses on Fort Polk, Louisiana.. Vet Parasitol Reg Stud Reports 2018 Aug;13:14-17.
    doi: 10.1016/j.vprsr.2018.03.002pubmed: 31014862google scholar: lookup
  84. Nielsen MK, Vidyashankar AN, Olsen SN, Monrad J, Thamsborg SM. Strongylus vulgaris associated with usage of selective therapy on Danish horse farms-is it reemerging?. Vet Parasitol 2012 Oct 26;189(2-4):260-6.
    doi: 10.1016/j.vetpar.2012.04.039pubmed: 22703964google scholar: lookup
  85. Jürgenschellert L, Krücken J, Austin CJ, Lightbody KL, Bousquet E, von Samson-Himmelstjerna G. Investigations on the occurrence of tapeworm infections in German horse populations with comparison of different antibody detection methods based on saliva and serum samples.. Parasit Vectors 2020 Sep 10;13(1):462.
    doi: 10.1186/s13071-020-04318-5pmc: PMC7488081pubmed: 32912340google scholar: lookup
  86. Barda BD, Rinaldi L, Ianniello D, Zepherine H, Salvo F, Sadutshang T, Cringoli G, Clementi M, Albonico M. Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field.. PLoS Negl Trop Dis 2013;7(8):e2344.
  87. Cringoli G, Maurelli MP, Levecke B, Bosco A, Vercruysse J, Utzinger J, Rinaldi L. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals.. Nat Protoc 2017 Sep;12(9):1723-1732.
    doi: 10.1038/nprot.2017.067pubmed: 28771238google scholar: lookup
  88. Noel ML, Scare JA, Bellaw JL, Nielsen MK. Accuracy and precision of Mini-FLOTAC and McMaster techniques for determining equine strongyle egg counts.. J Equine Vet Sci (2017) 48:182–7.e1.
  89. Rehbein S, Lindner T, Visser M, Winter R. Evaluation of a double centrifugation technique for the detection of Anoplocephala eggs in horse faeces.. J Helminthol 2011 Dec;85(4):409-14.
    doi: 10.1017/S0022149X10000751pubmed: 21138608google scholar: lookup
  90. Demeler J, Ramünke S, Wolken S, Ianiello D, Rinaldi L, Gahutu JB, Cringoli G, von Samson-Himmelstjerna G, Krücken J. Discrimination of gastrointestinal nematode eggs from crude fecal egg preparations by inhibitor-resistant conventional and real-time PCR.. PLoS One 2013;8(4):e61285.
  91. Gehlen H, Wulke N, Ertelt A, Nielsen MK, Morelli S, Traversa D, Merle R, Wilson D, Samson-Himmelstjerna GV. Comparative Analysis of Intestinal Helminth Infections in Colic and Non-Colic Control Equine Patients.. Animals (Basel) 2020 Oct 19;10(10).
    doi: 10.3390/ani10101916pmc: PMC7603170pubmed: 33086590google scholar: lookup
  92. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool.. J Mol Biol 1990 Oct 5;215(3):403-10.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  93. Howe KL, Bolt BJ, Shafie M, Kersey P, Berriman M. WormBase ParaSite - a comprehensive resource for helminth genomics.. Mol Biochem Parasitol 2017 Jul;215:2-10.
  94. . Comparative genomics of the major parasitic worms.. Nat Genet 2019 Jan;51(1):163-174.
    doi: 10.1038/s41588-018-0262-1pmc: PMC6349046pubmed: 30397333google scholar: lookup
  95. Collobert-Laugier C, Hoste H, Sevin C, Dorchies P. Prevalence, abundance and site distribution of equine small strongyles in Normandy, France.. Vet Parasitol 2002 Dec 11;110(1-2):77-83.
    doi: 10.1016/S0304-4017(02)00328-Xpubmed: 12446091google scholar: lookup
  96. Morariu S, Mederle N, Badea C, Dărăbuş G, Ferrari N, Genchi C. The prevalence, abundance and distribution of cyathostomins (small stongyles) in horses from Western Romania.. Vet Parasitol 2016 Jun 15;223:205-9.
    doi: 10.1016/j.vetpar.2016.04.021pubmed: 27198801google scholar: lookup
  97. Denwood MJ, Love S, Innocent GT, Matthews L, McKendrick IJ, Hillary N, Smith A, Reid SW. Quantifying the sources of variability in equine faecal egg counts: implications for improving the utility of the method.. Vet Parasitol 2012 Aug 13;188(1-2):120-6.
    doi: 10.1016/j.vetpar.2012.03.005pubmed: 22469484google scholar: lookup
  98. Slocombe JO, McCraw BM. Gastrointestinal nematodes in horses in Ontario.. Can Vet J 1973 May;14(5):101-5.
    pmc: PMC1696110pubmed: 4703606
  99. McCraw BM, Slocombe JO. Strongylus vulgaris in the horse: a review.. Can Vet J 1976 Jun;17(6):150-7.
    pmc: PMC1697226pubmed: 779947
  100. Ogbourne CP. Variations in the fecundity of strongylid worms of the horse.. Parasitology 1971 Oct;63(2):289-98.
    doi: 10.1017/S0031182000079609pubmed: 5129804google scholar: lookup
  101. Hedberg-Alm Y, Penell J, Riihimäki M, Osterman-Lind E, Nielsen MK, Tydén E. Parasite Occurrence and Parasite Management in Swedish Horses Presenting with Gastrointestinal Disease-A Case-Control Study.. Animals (Basel) 2020 Apr 7;10(4).
    doi: 10.3390/ani10040638pmc: PMC7222828pubmed: 32272754google scholar: lookup
  102. Nielsen MK, Vidyashankar AN, Bellaw J, Gravatte HS, Cao X, Rubinson EF, Reinemeyer CR. Serum Strongylus vulgaris-specific antibody responses to anthelmintic treatment in naturally infected horses.. Parasitol Res 2015 Feb;114(2):445-51.
    doi: 10.1007/s00436-014-4201-5pubmed: 25358238google scholar: lookup
  103. Klei TR, Chapman MR. Immunity in equine cyathostome infections.. Vet Parasitol 1999 Aug 31;85(2-3):123-33; discussion 133-6, 215-25.
    doi: 10.1016/S0304-4017(99)00093-Xpubmed: 10485359google scholar: lookup
  104. 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 2010 Dec 15;174(3-4):285-91.
    doi: 10.1016/j.vetpar.2010.09.007pubmed: 20933334google scholar: lookup
  105. Lester HE, Spanton J, Stratford CH, Bartley DJ, Morgan ER, Hodgkinson JE, Coumbe K, Mair T, Swan B, Lemon G, Cookson R, Matthews JB. Anthelmintic efficacy against cyathostomins in horses in Southern England.. Vet Parasitol 2013 Oct 18;197(1-2):189-96.
    doi: 10.1016/j.vetpar.2013.06.009pubmed: 23830687google scholar: lookup
  106. Sangster NC. Managing parasiticide resistance.. Vet Parasitol 2001 Jul 12;98(1-3):89-109.
    doi: 10.1016/S0304-4017(01)00425-3pubmed: 11516581google scholar: lookup

Citations

This article has been cited 2 times.
  1. Stummer M, Frisch V, Glitz F, Hinney B, Spergser J, Krücken J, Diekmann I, Dimmel K, Riedel C, Cavalleri JV, Rümenapf T, Joachim A, Lyrakis M, Auer A. Presence of Equine and Bovine Coronaviruses, Endoparasites, and Bacteria in Fecal Samples of Horses with Colic.. Pathogens 2023 Aug 15;12(8).
    doi: 10.3390/pathogens12081043pubmed: 37624003google scholar: lookup
  2. Onder Z, Yildirim A, Duzlu O, Ciloglu A, Yetismis G, Karabulut F, Inci A. Detection of SNPs and benzimidazole resistance in strongyle nematode eggs of horses by allele-specific PCR.. Parasitol Res 2023 Sep;122(9):2037-2043.
    doi: 10.1007/s00436-023-07903-6pubmed: 37354256google scholar: lookup