Anthelmintic resistance in equine parasites - detection, potential clinical relevance and implications for control

Veterinary Parasitology

Volumn 185, Issue 1, 2012, Pages 2-8

  Von Samson Himmelstjerna, Georg ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Cyathostomin; Horse; Parascaris equorum; Worm control

Indexed keywords

1,2,3,4 TETRAHYDROPYRIMIDINE DERIVATIVE; ANTHELMINTIC AGENT; BENZIMIDAZOLE DERIVATIVE; FENBENDAZOLE; IVERMECTIN; MACROLIDE; MOXIDECTIN; PYRANTEL;

AGRICULTURAL MANAGEMENT; ANTHELMINTIC RESISTANCE; ARTICLE; ASCARIDIA; CLINICAL EFFECTIVENESS; CYATHOSTOMIN DISEASE; CYATHOTOMIN; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE SEVERITY; DRUG EFFICACY; DRUG RESISTANCE; HORSE; HOST PARASITE INTERACTION; IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; INFECTION RISK; NONHUMAN; PARACARIS EQUORUM; PARASITE CONTROL; PARASITE EXAMINATION; PARASITE IDENTIFICATION; PARASITOSIS; PASTURE; RISK ASSESSMENT; RISK FACTOR; RISK REDUCTION; SMALL INTESTINE OBSTRUCTION; STRONGYLOIDEA;

ANIMALS; ANTHELMINTICS; DRUG RESISTANCE; HORSE DISEASES; HORSES; NEMATODA; NEMATODE INFECTIONS;

EQUIDAE; NEMATODA; PARASCARIS EQUORUM;

EID: 84856808749     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2011.10.010     Document Type: Article

References (80)

1. Bielza P., Quinto V., Gravalos C., Fernandez E., Abellan J., Contreras J. Stability of spinosad resistance in Frankliniella occidentalis (Pergande) under laboratory conditions. Bull. Entomol. Res. 2008, 98:355-359.
2. Boersema J.H., Eysker M., Nas J.W. Apparent resistance of Parascaris equorum to macrocylic lactones. Vet. Rec. 2002, 150:279-281.
3. Blackhall W.J., 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, 109:1199-1203.
4. - transport in the rat large intestine. Parasitol. Res. 2004, 92:490-495.
5. Clayton H.M., Duncan J.L. The development of immunity to Parascaris equorum infection in the foal. Res. Vet. Sci. 1979, 26:383-384.
6. Coles G.C., Bauer C., Borgsteede F.H., Geerts S., Klei T.R., Taylor M.A., Waller P.J. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 1992, 44:35-44.
7. Coles G.C., Jackson F., Pomroy W.E., Prichard R.K., von Samson-Himmelstjerna G., Silvestre A., Taylor M.A., Vercruysse J. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 2006, 136:167-185.
8. Craven J., Bjorn H., Barnes E.H., Henriksen S.A., Nansen P. A comparison of in vitro tests and a faecal egg count reduction test in detecting anthelmintic resistance in horse strongyles. Vet. Parasitol. 1999, 85:49-59.
9. Cobb R., Boeckh A. Moxidectin: a review of chemistry, pharmacokinetics and use in horses. Parasites & Vectors 2009, 2(2 Suppl.):S5.
10. Collobert-Laugier C., Hoste H., Sevin C., Dorchies P. Prevalence, abundance and site distribution of equine small strongyles in Normandy, France. Vet. Parasitol. 2002, 110:77-83.
11. Cribb N.C., Cote N.M., Boure L.P., Peregrine A.S. Acute small intestinal obstruction associated with Parascaris equorum infection in young horses: 25 cases (1985-2004). N. Z. Vet. J 2006, 54:338-343.
12. DiPietro J., Lock T., Todd K.S., Reuter J.V. Evaluation of ivermectin paste in the treatment of ponies for Parascaris equorum infections. J. Am. Vet. Med. Assoc. 1987, 190:1181-1183.
13. DiPietro J.A., Todd K.S. Anthelmintics used in treatment of parasitic infections of horses. Vet. Clin. North Am. Equine Pract. 1987, 3:1-14.
14. Drogemuller M., Beelitz P., Pfister K., Schnieder T., von Samson-Himmelstjerna G. Amplification of ribosomal DNA of Anoplocephalidae: Anoplocephala perfoliata diagnosis by PCR as a possible alternative to coprological methods. Vet. Parasitol. 2004, 124:205-215.
15. Drogemuller M., Schnieder T., von Samson-Himmelstjerna G. Evidence of p-glycoprotein sequence diversity in cyathostomins. J. Parasitol. 2004, 90:998-1003.
16. Duncan J.L., Bairden K., Abbott E.M. Elimination of mucosal cyathostome larvae by five daily treatments with fenbendazole. Vet. Rec. 1998, 142:268-271.
17. Edward C.L., Hoffmann A.A. Ivermectin resistance in a horse in Australia. Vet. Rec. 2008, 162:56-57.
18. Eysker M., Bakker J., van den Berg M., van Doorn D.C.K., Ploeger H.W. The use of age-clustered pooled faecal samples for monitoring worm control in horses. Vet. Parasitol. 2008, 151:249-255.
19. Eysker M., Boersema J.H., Kooyman F.N. Effect of early season ivermectin and pyrantel treatments on strongylid infections in young Shetland ponies in The Netherlands. Vet. Parasitol. 1991, 38:33-39.
20. French D., Klei T., Taylor H., Chapman M., Wright F. Efficacy of ivermectin in the oral paste formulation against naturally acquired adult and larval stages of Parascaris equorum in pony foals. Am. J. Vet. Res. 1988, 49:1000-1003.
21. 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, 42:79-83.
22. Gawor J.J. The prevalence and abundance of internal parasites in working horses autopsied in Poland. Vet. Parasitol. 1995, 58:99-108.
23. Hearn F.P., Peregrine A.S. Identification of foals infected with Parascaris equorum apparently resistant to ivermectin. J. Am. Vet. Med. Assoc. 2003, 223:482-485. 455.
24. Herd R.P. Parasite control in horses: pasture sweeping. Mod. Vet. Pract. 1986, 67:893-894.
25. Herd R.P. The changing world of worms: the rise of the Cyathostomomes and the decline of Strongylus vulgaris. Comp. Cont. Educ. Pract. Vet. 1990, 12:732-734.
26. Hodgkinson J.E., Clark H.J., Kaplan R.M., Lake S.L., Matthews J.B. The role of polymorphisms at beta tubulin isotype 1 codons 167 and 200 in benzimidazole esistance in cyathostomins. Int. J. Parasitol. 2008, 38:1149-1160.
27. Ihler C.F. A field survey on anthelmintic resistance in equine small strongyles in Norway. Acta Vet. Scand. 1995, 36:135-143.
28. Ihler C.F., Bjorn H. Use of two in vitro methods for the detection of benzimidazole resistance in equine small strongyles (Cyathostoma spp.). Vet. Parasitol. 1996, 65:117-125.
29. Jackson F., Coop R.L. The development of anthelmintic resistance in sheep nematodes. Parasitology 2000, 120(Suppl.):S95-S107.
30. Kaplan R.M. Anthelmintic resistance in nematodes of horses. Vet. Res. 2002, 33:491-507.
31. Kaplan R.M. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol. 2004, 20:477-481.
32. Kaplan R.M., Klei T.R., Lyons E.T., Lester G., Courtney C.H., French D.D., Tolliver S.C., Vidyashankar A.N., Zhao Y. Prevalence of anthelmintic resistant cyathostomes on horse farms. J. Am. Vet. Med. Assoc. 2004, 225:903-910.
33. Konigova A., Varady M., Corba J. Comparison of in vitro methods and faecal egg count reduction test for the detection of benzimidazole resistance in small strongyles of horses. Vet. Res. Commun. 2003, 27:281-288.
34. Krecek R.C., Guthrie A.J., Van Nieuwenhuizen L.C., Booth L.M. A comparison between the effects of conventional and selective antiparasitic treatments on nematode parasites of horses from two management schemes. J. S. Afr. Vet. Assoc. 1999, 65:97-100.
35. Kuzmina T.A., Kharchenko V.O. Anthelmintic resistance in cyathostomins of brood horses in Ukraine and influence of anthelmintic treatments on strongylid community structure. Vet. Parasitol. 2008, 154:277-288.
36. 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.
37. Lake, S.L., Matthews, J.B., Kaplan, R.M., Hodgkinson, J.E., 2009. Determination of genomic DNA sequences for beta-tubulin isotype 1 from multiple species of cyathostomin and detection of resistance alleles in third-stage larvae from horses with naturally acquired infections. Parasite & Vectors S 6.
38. Lind E.O., Kuzmina T., Uggla A., Waller P.J., Hoglund J. A field study on the effect of some anthelmintics on cyathostomins of horses in Sweden. Vet. Res. Commun. 2007, 31:53-65.
39. Lind E.O., Uggla A., Waller P., Hoglund J. Larval development assay for detection of anthelmintic resistance in cyathostomins of Swedish horses. Vet. Parasitol. 2005, 128:261-269.
40. Love S., Murphy D., Mellor D. Pathogenicity of cyathostome infection. Vet. Parasitol. 1999, 85:113-121.
41. Lyons E.T., Drudge J.H., Tolliver S.C., Granstrom D.E., Stamper S. Evaluation of exclusive use of ivermectin vs alternation of antiparasitic compounds for control of internal parasites of horses. Am. J. Vet. Res. 1992, 53:97-104.
42. Lyons E.T., Tolliver S.C., Collins S.S. Field studies on endoparasites of Thoroughbred foals on seven farms in central Kentucky in 2004. Parasitol. Res. 2006, 98:496-500.
43. Lyons E.T., Tolliver S.C., Rathgeber R.A., Collins S.S. Parasite field study in central Kentucky on thoroughbred foals (born in 2004) treated with pyrantel tartrate daily and other parasiticides periodically. Parasitol. Res. 2007, 100:473-478.
44. 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.
45. Lyons E.T., Tolliver S.C., Collins S.S. Probable reason why small strongyle EPG counts are returning "early" after ivermectin treatment of horses on a farm in Central Kentucky. Parasitol. Res. 2009, 104:569-574.
46. Lyons E.T., Tolliver S.C., Kuzmina T.A., Collins S.S. Critical tests evaluating efficacy of moxidectin against small strongyles in horses from a herd for which reduced activity had been found in field tests in Central Kentucky. Parasitol. Res. 2010, 107:1495-1498.
47. Marchiondo A.A., White G.W., Smith L.L., Reinemeyer C.R., Dascanio J.J., Johnson E.G., Shugart J.I. Clinical field efficacy and safety of pyrantel pamoate paste (19.13% w/w pyrantel base) against Anoplocephala spp. in naturally infected horses. Vet. Parasitol. 2006, 137:94-102.
48. Matthee S., McGeoch M.A. Helminths in horses: use of selective treatment for the control of strongyles. J. S. Afr. Vet. Assoc. 2004, 75:129-136.
49. Mercier P., Chick B., Alves-Branco F., White C.R. Comparative efficacy, persistent effect, and treatment intervals of anthelmintic pastes in naturally infected horses. Vet. Parasitol. 2001, 99:29-39.
50. Molento M.B., Antunes J., Bentes R.N., Coles G.C. Anthelmintic resistance in nematodes in Brazilian horses. Vet. Rec. 2008, 168:384-385.
51. 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.
52. Nielsen M.K., Baptiste K.E., Tolliver S.C., Collins S.S., Lyons E.T. 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. 2010, 174:77-84.
53. Pape M., Posedi J., Failing K., Schnieder T., von Samson-Himmelstjerna G. Analysis of the beta-tubulin codon 200 genotype distribution in a benzimidazole-susceptible and -resistant cyathostome population. Parasitology 2003, 127:53-59.
54. Pape M., Schnieder T., von Samson-Himmelstjerna G. Investigation of diversity and isotypes of the beta-tubulin cDNA in several small strongyle (Cyathostominae) species. J. Parasitol. 2002, 88:673-677.
55. Ploeger H.W., van Doorn D.C., Nijsse E.R., Eysker M. Decision trees on the web - a parasite compendium. Trends Parasitol. 2008, 24:203-204.
56. Rehbein S., Holste J.E., Doucet M.Y., Fenger C., Paul A.J., Reinemeyer C.R., Smith L.L., Yoon S., Marley S.E. Field efficacy of ivermectin plus praziquantel oral paste against naturally acquired gastrointestinal nematodes and cestodes of horses in North America and Europe. Vet. Ther. 2003, 4:220-227.
57. Reinemeyer C.R., Hutchens D.E., Eckblad W.P., Marchiondo A.A., Shugart J.I. Dose-confirmation studies of the cestocidal activity of pyrantel pamoate paste in horses. Vet. Parasitol. 2006, 138:234-239.
58. Ryu S.H., Jang J.D., Bak U.B., Lee C., Youn H.J., Lee Y.L. Gastrointestinal impaction by Parascaris equorum in a Thoroughbred foal in Jeju, Korea. J. Vet. Sci. 2004, 5:181-182.
59. Sangster N.C. Pharmacology of anthelmintic resistance in cyathostomes: will it occur with the avermectin/milbemycins?. Vet. Parasitol. 1999, 85:189-201. discussion 201-184, 215-125.
60. Schougaard H., Nielsen M.K. Apparent ivermectin resistance of Parascaris equorum in foals in Denmark. Vet. Rec. 2007, 160:439-440.
61. Slocombe J.O., Cote J.F., de Gannes R.V. The persistence of benzimidazole-resistant cyathostomes on horse farms in Ontario over 10 years and the effectiveness of ivermectin and moxidectin against these resistant strains. Can. Vet. J. 2008, 49:56-60.
62. Slocombe R. The trouble with life fluids: some parallels between mothers milk and lung juice. Vet. J. 2003, 165:5-6.
63. Steinbach T., Bauer C., Sasse H., Baumgärtner 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.
64. Tandon R., Kaplan R.M. Evaluation of a larval development assay (DrenchRite) for the detection of anthelmintic resistance in cyathostomin nematodes of horses. Vet. Parasitol. 2004, 121:125-142.
65. Traversa D., Klei T.R., Iorio R., Paoletti B., Lia R.P., Otranto D., Sparagano O.A., Giangaspero A. Occurrence of anthelmintic resistant equine cyathostome populations in central and southern Italy. Prev. Vet. Med. 2007, 82:314-320.
66. Traversa D., Iorio R., Otranto D., Giangaspero A., Milillo P., Klei T.R. Species-specific identification of equine cyathostomes resistant to fenbendazole and susceptible to oxibendazole and moxidectin by macroarray probing. Exp. Parasitol. 2009, 121:92-95.
67. Traversa, D., von Samson-Himmelstjerna, G., Demeler, J., Milillo, P., Schurmann, S., Barnes, H., Otranto, D., Perrucci, S., di Regalbono, A.F., Beraldo, P., Boeckh, A., Cobb, R., 2009b. Anthelmintic resistance in cyathostomin populations from horse yards in Italy, United Kingdom and Germany. Parasites & Vectors S 2.
68. Traversa D., Milillo P., Barnes H., von Samson-Himmelstjerna G., Schurmann S., Demeler J., Otranto D., Lia R.P., Perrucci S., Frangipane di Regalbono A., Beraldo P., Amodie D., Rohn K., Cobb R., Boeckh A. Distribution and species-specific occurrence of cyathostomins (Nematoda, Strongylida) in naturally infected horses from Italy United Kingdom and Germany. Vet. Parasitol. 2010, 168:84-92.
69. Trawford A.F., Burden F., Hodgkinson J.E. Suspected moxidectin resistance in cyathostomes in two donkey herds at the Donkey Sanctuary, UK. Proc 20th Int. Conf. World Assoc. Adv. Vet. Parasitol. 2005.
70. Valdez R.A., DiPietro J.A., Paul A.J., Lock T.F., Hungerford L.L., Todd K.S. Controlled efficacy study of the bioequivalence of Strongid C and generic pyrantel tartrate in horses. Vet. Parasitol. 1995, 60:83-102.
71. van Doorn D.C.K., Lerns S., Weteling A., Ploeger H.W., Eysker M. Resistance of Parascaris equourm against ivermection due to frequent anthelmintic treatment of. foals in The Netherlands. Proc 21st Int. Conf. World. Assoc. Adv. Vet. Parasitol. 2007.
72. Vidyashankar A.N., Hanlon B.M., Kaplan R.M. Statistical and biological considerations in evaluating drug efficacy in equine strongyle parasites using fecal egg count data. Vet. Parasitol. 2012, 185:45-56.
73. von Samson-Himmelstjerna G., Buschbaum S., Wirtherle N., Pape M., Schnieder T. TaqMan minor groove binder real-time PCR analysis of beta-tubulin codon 200 polymorphism in small strongyles (Cyathostomin) indicates that the TAC allele is only moderately selected in benzimidazole-resistant populations. Parasitology 2003, 127:489-496.
74. von Samson-Himmelstjerna G. Molecular diagnosis of anthelmintic resistance. Vet. Parasitol. 2006, 136:99-107.
75. von Samson-Himmelstjerna G., Blackhall W.J., McCarthy J.S., Skuce P.J. Single nucleotide polymorphism (SNP) markers for benzimidazole resistance in veterinary nematodes. Parasitology 2007, 134:1077-1086.
76. von Samson-Himmelstjerna G., Fritzen B., Demeler J., Schurmann 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.
77. von Samson-Himmelstjerna G., Coles G.C., Jackson F., Bauer C., Borgsteede F.M., Cirak V.Y., Demeler J., Donnan A., Dorny P., Epe C., Harder A., Höglund J., Kaminsky R., Kerboeuf D., Küttler U., Papadopoulos E., Posedi J., Small J., Várady M., Vercruysse J., Wirtherle N. Standardization of the egg hatch test for the detection of benzimidazole resistance in parasitic nematodes. Parasitol. Res. 2009, 105:825-834.
78. Wirtherle N., Schnieder T., von Samson-Himmelstjerna G. Prevalence of benzimidazole resistance on horse farms in Germany. Vet. Rec. 2004, 154:39-41.
79. Wolstenholme A.J., Fairweather I., Prichard R., von Samson-Himmelstjerna G., Sangster N.C. Drug resistance in veterinary helminths. Trends Parasitol. 2004, 20:469-476.
80. Young K.E., Garza V., Snowden K., Dobson R.J., Powell D., Craig T.M. Parasite diversity and anthelmintic resistance in two herds of horses. Vet. Parasitol. 1999, 85:205-214. discussion 215-225.