An update on cyathostomins: Anthelmintic resistance and diagnostic tools

Equine Veterinary Journal

Volumn 43, Issue SUPPL.39, 2011, Pages 133-139

  Stratford, C H ^a   McGorum, B C ^a   Pickles, K J ^b   Matthews, J B ^c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MOREDUN RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Anthelmintic resistance; Cyathostomin; Diagnostic tools; Horse; Sensitivity testing

Indexed keywords

ANTHELMINTIC AGENT;

ANIMAL; ANIMAL DISEASE; DRUG EFFECT; DRUG RESISTANCE; HORSE; HORSE DISEASE; NEMATODE; NEMATODIASIS; PARASITOLOGY; REVIEW;

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

EQUIDAE; NEMATODA;

EID: 79960726397     PISSN: 04251644     EISSN: 20423306     Source Type: Journal    
DOI: 10.1111/j.2042-3306.2011.00397.x     Document Type: Review

References (82)

1. Bairden, K., Davies, H.S., Gibson, N.R., Hood, A.J. and Parker, L.D. (2006) Efficacy of moxidectin 2 per cent oral gel against cyathostomins, particularly third-stage inhibited larvae, in horses. Vet. Rec. 158, 766-767.
2. Becher, A.M., Mahling, M., Nielsen, M.K. and Pfister, K. (2010) Selective anthelmintic therapy of horses in the Federal states of Bavaria (Germany) and Salzburg (Austria): An investigation into strongyle egg shedding consistency. Vet. Parasitol. 171, 116-122.
3. Bello, T.R. and Allen, T.M. (2009) Comparison of two fecal egg recovery techniques and larval culture for cyathostomins in horses. Am. J. vet. Res. 70, 571-573.
4. Borgsteede, F.H., Boersma, J.H., Gaasenbeek, C.P. and van der Burg, W.P. (1993) The reappearance of eggs in faeces of horses after treatment with ivermectin. Vet. Q. 15, 24-26.
5. Braga, F.R., Araujo, J.V., Carvalho, R.O., Silva, A.R., Araujo, J.M., Soares, F.E., Genier, H.L., Ferreira, S.R. and Queiroz, J.H. (2010a) Ovicidal action of a crude enzymatic extract of the fungus Pochonia chlamydosporia against cyathostomin eggs. Vet. Parasitol. 172, 264-268.
6. Braga, F.R., Araujo, J.V., Silva, A.R., Carvalho, R.O., Araujo, J.M., Ferreira, S.R. and Carvalho, G.R. (2010b) Viability of the nematophagous fungus Pochonia chlamydosporia after passage through the gastrointestinal tract of horses. Vet. Parasitol. 168, 264-268.
7. Chandler, K.J. and Love, S. (2002) Patterns of equine faecal egg counts following spring dosing with either fenbendazole or moxidectin. Vet. Rec. 151, 269-270.
8. Chandler, K.J., Collins, M.C. and Love, S. (2000) Efficacy of a five-day course of fenbendazole in benzimidazole-resistant cyathostomes. Vet. Rec. 147, 661-662.
9. Clark, H.J., Kaplan, R.M., Matthews, J.B. and Hodgkinson, J.E. (2005) Isolation and characterisation of a beta tubulin isotype 2 gene from two species of cyathostomin. Int. J. Parasitol. 35, 349-358.
10. Coles, G.C., Jackson, F., Pomroy, W.E., Prichard, R.K., von Samson-Himmelstjerna, G., Silvestre, A., Taylor, M.A. and Vercruysse, J. (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 136, 167-185.
11. Colglazier, M.L., Enzie, F.D. and Kates, K.C. (1977) Critical anthelmintic trials in ponies with four benzimidazoles: Mebendazole, cambendazole, fenbendazole, and albendazole. J. Parasitol. 63, 724-727.
12. Comer, K.C., Hillyer, M.H. and Coles, G.C. (2006) Anthelmintic use and resistance on Thoroughbred training yards in the UK. Vet. Rec. 158, 596-598.
13. Craven, J., Bjorn, H., Barnes, E.H., Henriksen, S.A. and Nansen, P. (1999) A comparison of in vitro tests and a faecal egg count reduction test in detecting anthelmintic resistance in horse strongyles. Vet. Parasitol. 85, 49-59.
14. Craven, J., Bjorn, H., Henriksen, S.A., Nansen, P., Larsen, M. and Lendal, S. (1998) Survey of anthelmintic resistance on Danish horse farms, using 5 different methods of calculating faecal egg count reduction. Equine vet. J. 30, 289-293.
15. Dargatz, D.A., Traub-Dargatz, J.L. and Sangster, N.C. (2000) Antimicrobic and anthelmintic resistance. Vet. Clin. N. Am.: Equine Pract. 16, 515-536, ix-x.
16. Dipietro, J. (1992) Daily anthelmintic therapy in horses. Comp. cont. Educ. pract. Vet. 14, 651-654.
17. Dowdall, S.M., Proudman, C.J., Klei, T.R., Mair, T. and Matthews, J.B. (2004) Characterisation of IgG(T) serum antibody responses to two larval antigen complexes in horses naturally- or experimentally-infected with cyathostomins. Int. J. Parasitol. 34, 101-108.
18. Dowdall, S.M., Proudman, C.J., Love, S., Klei, T.R. and Matthews, J.B. (2003) Purification and analyses of the specificity of two putative diagnostic antigens for larval cyathostomin infection in horses. Res. vet. Sci. 75, 223-229.
19. Dowdall, S.M., Matthews, J.B., Mair, T., Murphy, D., Love, S. and Proudman, C.J. (2002) Antigen-specific IgG(T) responses in natural and experimental cyathostominae infection in horses. Vet. Parasitol. 106, 225-242.
20. Drudge, J.H., Lyons, E.T. and Tolliver, S.C. (1979) Benzimidazole resistance of equine stronygles - critical tests of six compounds against population B. Am. J. vet. Res. 40, 590-594.
21. Duncan, J.L. (1974) Field studies on the epidemiology of mixed strongyle infection in the horse. Vet. Rec. 94, 337-345.
22. Duncan, J.L. (1985) Internal parasites of the horse and their control. Equine vet. J. 17, 79-82.
23. Duncan, J.L. and Love, S. (1991) Preliminary observations on an alternative strategy for the control of horse strongyles. Equine vet. J. 23, 226-228.
24. Duncan, J.L., Bairden, K. and Abbott, E.M. (1998) Elimination of mucosal cyathostome larvae by five daily treatments with fenbendazole. Vet. Rec. 142, 268-271.
25. Earle, C.G., Kington, H.A. and Coles, G.C. (2002) Helminth control used by trainers of Thoroughbreds in England. Vet. Rec. 150, 405-408.
26. Eysker, M., Boersema, J.H., Grinwis, G.C., Kooyman, F.N. and Poot, J. (1997) Controlled dose confirmation study of a 2% moxidectin equine gel against equine internal parasites in The Netherlands. Vet. Parasitol. 70, 165-173.
27. Gilleard, J.S. and Beech, R.N. (2007) Population genetics of anthelmintic resistance in parasitic nematodes. Parasitol. 134, 1133-1147.
28. Gomez, H.H. and Georgi, J.R. (1991) Equine helminth infections: Control by selective chemotherapy. Equine vet. J. 23, 198-200.
29. Herd, R.P. (1986) Epidemiology and control of equine strongylosis at Newmarket. Equine vet. J. 18, 447-452.
30. Herd, R.P. and Gabel, A.A. (1990) Reduced efficacy of anthelmintics in young compared with adult horses. Equine vet. J. 22, 164-169.
31. Hillyer, M.H. and Mair, T.S. (1997) Recurrent colic in the mature horse: A retrospective review of 58 cases. Equine vet. J. 29, 421-424.
32. Hodgkinson, J.E., Clark, H.J., Kaplan, R.M., Lake, S.L. and Matthews, J.B. (2008) The role of polymorphisms at beta tubulin isotype 1 codons 167 and 200 in benzimidazole resistance in cyathostomins. Int. J. Parasitol. 38, 1149-1160.
33. Jackson, F. and Coop, R.L. (2000) The development of anthelmintic resistance in sheep nematodes. Parasitol. 120, 95-107.
34. Kaplan, R.M. (2002) Anthelmintic resistance in nematodes of horses. Vet. Res. 33, 491-507.
35. Kaplan, R.M. and Nielsen, M.K. (2010) An evidence-based approach to equine parasite control: It ain't the 60s anymore. Equine vet. Educ. 22, 306-316.
36. Kaplan, R.M., Klei, T.R., Lyons, E.T., Lester, G., Courtney, C.H., French, D.D., Tolliver, S.C., Vidyashankar, A.N. and Zhao, Y. (2004) Prevalence of anthelmintic resistant cyathostomes on horse farms. J. Am. vet. med. Ass. 225, 903-910.
37. Klei, T.R., Chapman, M.R., French, D.D. and Taylor, H.W. (1993) Evaluation of ivermectin at an elevated dose against encysted equine cyathostome larvae. Vet. Parasitol. 47, 99-106.
38. Konigova, A., Varady, M. and Corba, J. (2003) 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. 27, 281-288.
39. Lake, S.L., Matthews, J.B., Kaplan, R.M. and 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. Parasit Vectors 2 Suppl. 2, S6.
40. LeJambre, L.F. (1976) Egg hatch as an in vitro assay of thiabendazole resistance in nematodes. Vet. Parasitol. 2, 385-391.
41. Lloyd, S. (2009) Effects of previous control programmes on the proportion of horses shedding small numbers of strongyle-type eggs. Vet. Rec. 164, 108-111.
42. Love, S. and McKeand, J. (1997) Cyathostominosis: Practical issues of treatment and control. Equine vet. Educ. 9, 253-256.
43. Love, S., Murphy, D. and Mellor, D. (1999) Pathogenicity of cyathostome infection. Vet. Parasitol. 85, 113-121, discussion 121-112, 215-125.
44. Lyons, E.T., Drudge, J.H. and Tolliver, S.C. (2000) Larval cyathostomiasis. Vet. Clin. N. Am.: Equine Pract. 16, 501-513.
45. Lyons, E.T., Tolliver, S.C. and Drudge, J.H. (1999) Historical perspective of cyathostomes: Prevalence, treatment and control programs. Vet. Parasitol. 85, 97-111, discussion 111-112, 215-125.
46. Lyons, E.T., Drudge, J.H., Tolliver, S.C. and Breukink, H.J. (1974) Critical test of three salts of pyrantel against internal parasites of the horse. Am. J. vet. Res. 35, 1515-1522.
47. Lyons, E.T., Tolliver, S.C., Ionita, M., Lewellen, A. and Collins, S.S. (2008) Field studies indicating reduced activity of ivermectin on small strongyles in horses on a farm in Central Kentucky. Parasitol. Res. 103, 209-215.
48. Martin, P.J., Anderson, N. and Jarrett, R.G. (1989) Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays. Aust. vet. J. 66, 236-240.
49. Matthews, J. (2008) An update on cyathostomins: Anthelmintic resistance and worm control. Equine vet. Educ. 20, 552-560.
50. Matthews, J.B., McArthur, C., Robinson, A. and Jackson, F. (2011) The in vitro diagnosis of anthelmintic resistance in cyathostomins. Vet. Parasitol. (in press).
51. McWilliam, H.E., Nisbet, A.J., Dowdall, S.M., Hodgkinson, J.E. and Matthews, J.B. (2010) Identification and characterisation of an immunodiagnostic marker for cyathostomin developing stage larvae. Int. J. Parasitol. 40, 265-275.
52. Mercier, P., Chick, B., Alves-Branco, F. and White, C.R. (2001) Comparative efficacy, persistent effect, and treatment intervals of anthelmintic pastes in naturally infected horses. Vet. Parasitol. 99, 29-39.
53. Miller, C.M., Waghorn, T.S., Leathwick, D.M. and Gilmour, M.L. (2006) How repeatable is a faecal egg count reduction test? N. Z. vet. J. 54, 323-328.
54. Molento, M.B., Antunes, J., Bentes, R.N. and Coles, G.C. (2008) Anthelmintic resistant nematodes in Brazilian horses. Vet. Rec. 162, 384-385.
55. Morgan, E.R., Hetzel, N., Povah, C. and Coles, G.C. (2005) Prevalence and diagnosis of parasites of the stomach and small intestine in horses in south-west England. Vet. Rec. 156, 597-600.
56. Murphy, D. and Love, S. (1997) The pathogenic effects of experimental cyathostome infections in ponies. Vet. Parasitol. 70, 99-110.
57. Nielsen, M.K. (2009) Restrictions of anthelmintic usage: Perspectives and potential consequences. Parasit Vectors 2 Suppl. 2, S7.
58. Nielsen, M.K., Haaning, N. and Olsen, S.N. (2006a) Strongyle egg shedding consistency in horses on farms using selective therapy in Denmark. Vet. Parasitol. 135, 333-335.
59. Nielsen, M.K., Monrad, J. and Olsen, S.N. (2006b) Prescription-only anthelmintics - a questionnaire survey of strategies for surveillance and control of equine strongyles in Denmark. Vet. Parasitol. 135, 47-55.
60. Nielsen, M.K., Vidyashankar, A.N., Andersen, U.V., Delisi, K., Pilegaard, K. and Kaplan, R.M. (2010) Effects of fecal collection and storage factors on strongylid egg counts in horses. Vet. Parasitol. 167, 55-61.
61. Ogbourne, C.P. (1976) The prevalence, relative abundance and site distribution of nematodes of the subfamily Cyathostominae in horses killed in Britain. J. Helminthol. 50, 203-214.
62. Osterman Lind, E., Kuzmina, T., Uggla, A., Waller, P. and Höglund, J. (2007) A field study on the effect of some anthelmintics on cyathostomins of horses in Sweden. Vet. Res. Commun. 31, 53-65.
63. Pickles, K.J., Mair, J.A., Lopez-Villalobos, N., Shaw, D.J., Scott, I. and Pomroy, W. (2010) Large intestinal mast cell count and proteinase expression is associated with larval burden in cyathostomin-infected horses. Equine vet. J. 42, 652-657.
64. Presland, S.L., Morgan, E.R. and Coles, G.C. (2005) Counting nematode eggs in equine faecal samples. Vet. Rec. 156, 208-210.
65. Prichard, R.K., Hall, C.A., Kelly, J.D., Martin, I.C. and Donald, A.D. (1980) The problem of anthelmintic resistance in nematodes. Aust. vet. J. 56, 239-251.
66. Reinemeyer, C.R., Farley, A.W. and Clymer, B.C. (2003) Comparisons of cyathostome control and selection for benzimidazole resistance using larvicidal regimens of moxidectin gel or fenbendazole paste. Int. J. Appl. Res. Vet. Med. 1, 66-72.
67. Reinemeyer, C.R., Smith, S.A., Gabel, A.A. and Herd, R.P. (1984) The prevalence and intensity of internal parasites of horses in the U.S.A. Vet. Parasitol. 15, 75-83.
68. Rossano, M.G., Smith, A.R. and Lyons, E.T. (2010) Shortened strongyle-type egg reappearance periods in naturally infected horses treated with moxidectin and failure of a larvicidal dose of fenbendazole to reduce fecal egg counts. Vet. Parasitol. 173, 349-352.
69. Sangster, N.C. (1999) Pharmacology of anthelmintic resistance in cyathostomes: Will it occur with the avermectin/milbemycins? Vet. Parasitol. 85, 189-201; discussion 201-184, 215-125.
70. Sangster, N. (2003) A practical approach to anthelmintic resistance. Equine vet. J. 35, 218-219.
71. Slocombe, J.O. and de Gannes, R.V. (2006) Cyathostomes in horses in Canada resistant to pyrantel salts and effectively removed by moxidectin. Vet. Parasitol. 140, 181-184.
72. Tarigo-Martinie, J.L., Wyatt, A.R. and Kaplan, R.M. (2001) Prevalence and clinical implications of anthelmintic resistance in cyathostomes of horses. J. Am. vet. med. Ass. 218, 1957-1960.
73. Taylor, M.A. and Hunt, K.R. (1989) Anthelmintic drug resistance in the UK. Vet. Rec. 125, 143-147.
74. Traversa, D., Klei, T.R., Iorio, R., Paoletti, B., Lia, R.P., Otranto, D., Sparagano, O.A. and Giangaspero, A. (2007) Occurrence of anthelmintic resistant equine cyathostome populations in central and southern Italy. Prev. vet. Med. 82, 314-320.
75. Trawford, A.F., Burden, F.A. and Hodgkinson, J. (2005) Suspected moxidectin resistance in cyathostomes in two donkey herds at The Donkey Sanctuary, UK. Proceedings of the 20th International Conference World Association for Advanced Veterinary Parasitology, New Zealand. p 196.
76. Uhlinger, C. (1990) Effects of three anthelmintic schedules on the incidence of colic in horses. Equine vet. J. 22, 251-254.
77. Uhlinger, C.A. (1993) Uses of fecal egg count data in equine practice. Comp. cont. Educ. pract. Vet. 15, 742-748.
78. Van Wyk, J.A., Malan, F.S., van Rensburg, L.J., Oberem, P.T. and Allan, M.J. (1997) Quality control in generic anthelmintics: Is it adequate? Vet. Parasitol. 72, 157-165.
79. von Samson-Himmelstjerna, G., Fritzen, B., Demeler, J., Schurmann, S., Rohn, K., Schnieder, T. and Epe, C. (2007) 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. 144, 74-80.
80. von Samson-Himmelstjerna, G., Traversa, D., Demeler, J., Rohn, K., Milillo, P., Schurmann, S., Lia, R., Perrucci, S., di Regalbono, A.F., Beraldo, P., Barnes, H., Cobb, R. and Boeckh, A. (2009) Effects of worm control practices examined by a combined faecal egg count and questionnaire survey on horse farms in Germany, Italy and the UK. Parasit Vectors 2 (Suppl. 2), S3.
81. Waller, P.J. (1987) Anthelmintic resistance and the future for roundworm control. Vet. Parasitol. 25, 177-191.
82. Xiao, L., Herd, R.P. and Majewski, G.A. (1994) Comparative efficacy of moxidectin and ivermectin against hypobiotic and encysted cyathostomes and other equine parasites. Vet. Parasitol. 53, 83-90.