Skip to main content
SpringerLink
Log in

Occurrence, Measurement and Clinical Perspectives of Drug Resistance in Important Parasitic Helminths of Livestock

  • Chapter
  • First Online:
Antimicrobial Drug Resistance

Abstract

Livestock parasite resistance to anthelmintics remains one of the major limitations to ongoing animal health, welfare and productivity worldwide. Subsequent less-than-optimal parasite control can impose significant direct and indirect costs within all production and recreation livestock enterprises.

This chapter briefly summarises the biology and epidemiology of the important nematode and trematode parasites of cattle, sheep and horses around the world. Then it details the application, including modes of action and specific mechanisms of resistance, of the key anthelmintic options to assist their control.

The general principles regarding the development of anthelmintic resistance are discussed in light of an understanding to assist the slowing of worsening spread and to support effective and sustainable helminth control. There is also discussion of methods to detect, measure and monitor anthelmintic resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Waller PJ. Global perspectives on nematode parasite control in ruminant livestock: the need to adopt alternatives to chemotherapy, with emphasis on biological control. Anim Health Res Rev. 2003;4(1):35–43.

    Article  PubMed  Google Scholar 

  2. Nieuwhof GJ, Bishop SC. Costs of the major endemic diseases of sheep in Great Britain and the potential benefits of reduction in disease impact. Anim Sci. 2005;81(1):23–9.

    Article  Google Scholar 

  3. Sutherland IA, Shaw J, Shaw RJ. The production costs of anthelmintic resistance in sheep managed within a monthly preventive drench program. Vet Parasitol. 2010;171(3–4):300–4.

    Article  CAS  PubMed  Google Scholar 

  4. Kaplan RM, Vidyashankar AN. An inconvenient truth: global worming and anthelmintic resistance. Vet Parasitol. 2012;186(1–2):70–8.

    Article  PubMed  Google Scholar 

  5. McLeod RS. Costs of major parasites to the Australian livestock industries. Int J Parasitol. 1995;25(11):1363–7.

    Article  CAS  PubMed  Google Scholar 

  6. Molina-Hernández V, Mulcahy G, Pérez J, Martínez-Moreno Á, Donnelly S, O’Neill SM, et al. Fasciola hepatica vaccine: we may not be there yet but we’re on the right road. Vet Parasitol. 2015;208(1–2):101–11.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kaplan RM. Fasciola hepatica: a review of the economic impact in cattle and considerations for control. Vet Ther. 2001;2(1):40–50.

    CAS  PubMed  Google Scholar 

  8. Waller PJ. From discovery to development: current industry perspectives for the development of novel methods of helminth control in livestock. Vet Parasitol. 2006;139(1–3):1–14.

    Article  CAS  PubMed  Google Scholar 

  9. Mezo M, Gonzalez-Warleta M, Castro-Hermida JA, Muino L, Ubeira FM. Association between anti-F. hepatica antibody levels in milk and production losses in dairy cows. Vet Parasitol. 2011;180(3–4):237–42.

    Article  PubMed  Google Scholar 

  10. Kahn LP, Woodgate RG. Integrated parasite management: products for adoption by the Australian sheep industry. Vet Parasitol. 2012;186(1–2):58–64.

    Article  CAS  PubMed  Google Scholar 

  11. Playford MC, Smith AN, Love S, Besier RB, Kluver P, Bailey JN. Prevalence and severity of anthelmintic resistance in ovine gastrointestinal nematodes in Australia (2009–2012). Aust Vet J. 2014;92(12):464–71.

    Article  CAS  PubMed  Google Scholar 

  12. Leathwick DM. Managing anthelmintic resistance—parasite fitness, drug use strategy and the potential for reversion towards susceptibility. Vet Parasitol. 2013;198(1–2):145–53.

    Article  CAS  PubMed  Google Scholar 

  13. Van Wyk JA, Malan FS, Randles JL. How long before resistance makes it impossible to control some field strains of Haemonchus contortus in South Africa with any of the modern anthelmintics? Vet Parasitol. 1997;70(1–3):111–22.

    PubMed  Google Scholar 

  14. Besier RB, Love SCJ. Anthelmintic resistance in sheep nematodes in Australia: the need for new approaches. Aust J Exp Agr. 2003;43(12):1383–91.

    Article  CAS  Google Scholar 

  15. Miller CM, Waghorn TS, Leathwick DM, Candy PM, Oliver AMB, Watson TG. The production cost of anthelmintic resistance in lambs. Vet Parasitol. 2012;186(3–4):376–81.

    Article  CAS  PubMed  Google Scholar 

  16. Sutherland IA, Leathwick DM. Anthelmintic resistance in nematode parasites of cattle: a global issue? Trends Parasitol. 2011;27(4):176–81.

    Article  PubMed  Google Scholar 

  17. Taylor MA. SCOPS and COWS—‘Worming it out of UK farmers’. Vet Parasitol. 2012;186(1–2):65–9.

    Article  CAS  PubMed  Google Scholar 

  18. Borges FA, Almeida GD, Heckler RP, Lemes RT, Onizuka MK, Borges DG. Anthelmintic resistance impact on tropical beef cattle productivity: effect on weight gain of weaned calves. Trop Anim Health Prod. 2013;45(3):723–7.

    Article  PubMed  Google Scholar 

  19. Kaplan RM, Nielsen MK. An evidence-based approach to equine parasite control: It ain’t the 60s anymore. Eq Vet Edu. 2010;22(6):306–16.

    Article  Google Scholar 

  20. von Samson-Himmelstjerna G. Anthelmintic resistance in equine parasites—detection, potential clinical relevance and implications for control. Vet Parasitol. 2012;185(1):2–8.

    Article  CAS  Google Scholar 

  21. Nielsen MK, Pfister K, von Samson-Himmelstjerna G. Selective therapy in equine parasite control—application and limitations. Vet Parasitol. 2014;202(3–4):95–103.

    Article  CAS  PubMed  Google Scholar 

  22. Kaplan RM, West EM, Norat-Collazo LM, Vargas J. A combination treatment strategy using pyrantel pamoate and oxibendazole demonstrates additive effects for controlling equine cyathostomins. Eq Vet Edu. 2014;26(9):485–91.

    Article  Google Scholar 

  23. Kotze AC, Hunt PW, Skuce P, von Samson-Himmelstjerna G, Martin RJ, Sager H, et al. Recent advances in candidate-gene and whole-genome approaches to the discovery of anthelmintic resistance markers and the description of drug/receptor interactions. Int J Parasitol Drugs Drug Resist. 2014;4(3):164–84.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Foreyt WJ. Efficacy and safety of albendazole against experimentally induced Fasciola hepatica infections in goats. Vet Parasitol. 1988;26(3–4):261–4.

    Article  CAS  PubMed  Google Scholar 

  25. Riviere JE, Papich MG. Veterinary pharmacology and therapeutics. Ames: Wiley; 2009.

    Google Scholar 

  26. Sangster NC, Prichard RK, Lacey E. Tubulin and benzimidazole-resistance in Trichostrongylus colubriformis (Nematoda). J Parasitol. 1985;645–651.

    Google Scholar 

  27. Sangster NC, Riley FL, Collins GH. Investigation of the mechanism of levamisole resistance in trichostrongylid nematodes of sheep. Int J Parasitol. 1988;18(6):813–8.

    Article  CAS  PubMed  Google Scholar 

  28. Barrere V, Beech RN, Charvet CL, Prichard RK. Novel assay for the detection and monitoring of levamisole resistance in Haemonchus contortus. Int J Parasitol. 2014;44(3-4):235–41.

    Article  CAS  PubMed  Google Scholar 

  29. Vercruysse J, Rew RS. Macrocyclic lactones in antiparasitic therapy. Wallingford: CABI; 2002.

    Book  Google Scholar 

  30. Lanusse C, Lifschitz A, Virkel G, Alvarez L, Sanchez S, Sutra JF, et al. Comparative plasma disposition kinetics of ivermectin, moxidectin and doramectin in cattle. J Vet Pharmacol Ther. 1997;20(2):91–9.

    Article  CAS  PubMed  Google Scholar 

  31. Alvinerie M, Escudero E, Sutra J-F, Eeckhoutte C, Galtier P. The pharmacokinetics of moxidectin after oral and subcutaneous administration to sheep. Vet Res. 1998;29(2):113–8.

    CAS  PubMed  Google Scholar 

  32. Klei TR, Chapman MR, French DD, Taylor HW. Evaluation of ivermectin at an elevated dose against encysted equine cyathostome larvae. Vet Parasitol. 1993;47(1–2):99–106.

    Article  CAS  PubMed  Google Scholar 

  33. Xiao L, Herd RP, Majewski GA. Comparative efficacy of moxidectin and ivermectin against hypobiotic and encysted cyathostomes and other equine parasites. Vet Parasitol. 1994;53(1–2):83–90.

    Article  CAS  PubMed  Google Scholar 

  34. 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;63(3–4):225–35.

    Article  CAS  PubMed  Google Scholar 

  35. Steinbach T, Bauer C, Sasse H, Baumgärtner W, Rey-Moreno C, Hermosilla C, et al. Small strongyle infection: consequences of larvicidal treatment of horses with fenbendazole and moxidectin. Vet Parasitol. 2006;139(1–3):115–31.

    Article  CAS  PubMed  Google Scholar 

  36. Demeler J, Kuttler U, El-Abdellati A, Stafford K, Rydzik A, Varady M, et al. Standardization of the larval migration inhibition test for the detection of resistance to ivermectin in gastro intestinal nematodes of ruminants. Vet Parasitol. 2010;174(1–2):58–64.

    Article  CAS  PubMed  Google Scholar 

  37. Freeman AS, Nghiem C, Li J, Ashton FT, Guerrero J, Shoop WL, et al. Amphidial structure of ivermectin-resistant and susceptible laboratory and field strains of Haemonchus contortus. Vet Parasitol. 2003;110(3-4):217–26.

    Article  CAS  PubMed  Google Scholar 

  38. Dent JA, Smith MM, Vassilatis DK, Avery L. The genetics of ivermectin resistance in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2000;97(6):2674–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Urdaneta-Marquez L, Bae SH, Janukavicius P, Beech R, Dent J, Prichard R. A dyf-7 haplotype causes sensory neuron defects and is associated with macrocyclic lactone resistance worldwide in the nematode parasite Haemonchus contortus. Int J Parasitol. 2014;44(14):1063–71.

    Article  CAS  PubMed  Google Scholar 

  40. Kaminsky R, Ducray P, Jung M, Clover R, Rufener L, Bouvier J, et al. A new class of anthelmintics effective against drug-resistant nematodes. Nature. 2008;452(7184):176–80.

    Article  CAS  PubMed  Google Scholar 

  41. Lecova L, Stuchlikova L, Prchal L, Skalova L. Monepantel: the most studied new anthelmintic drug of recent years. Parasitology. 2014;141(13):1686–98.

    Article  CAS  PubMed  Google Scholar 

  42. Hosking BC, Dobson DP, Stein PA, Kaminsky R, Bapst B, Mosimann D, et al. Dose confirmation studies for monepantel, an amino-acetonitrile derivative, against fourth stage gastro-intestinal nematode larvae infecting sheep. Vet Parasitol. 2009;160(3–4):251–7.

    Article  CAS  PubMed  Google Scholar 

  43. Sager H, Hosking B, Bapst B, Stein P, Vanhoff K, Kaminsky R. Efficacy of the amino-acetonitrile derivative, monepantel, against experimental and natural adult stage gastro-intestinal nematode infections in sheep. Vet Parasitol. 2009;159(1):49–54.

    Article  CAS  PubMed  Google Scholar 

  44. Kaminsky R, Gauvry N, Schorderet Weber S, Skripsky T, Bouvier J, Wenger A, et al. Identification of the amino-acetonitrile derivative monepantel (AAD 1566) as a new anthelmintic drug development candidate. Parasitol Res. 2008;103(4):931–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Stein PA, George SD, Rolfe PF, Hosking BC. Safety and efficacy against fourth-stage gastrointestinal nematode larvae, of monepantel in 6-week old lambs. Vet Parasitol. 2012;185(2-4):339–42.

    Article  CAS  PubMed  Google Scholar 

  46. Rufener L, Maser P, Roditi I, Kaminsky R. Haemonchus contortus acetylcholine receptors of the DEG-3 subfamily and their role in sensitivity to monepantel. PLoS Pathog. 2009;5(4):e1000380.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Rufener L, Baur R, Kaminsky R, Maser P, Sigel E. Monepantel allosterically activates DEG-3/DES-2 channels of the gastrointestinal nematode Haemonchus contortus. Mol Pharmacol. 2010;78(5):895–902.

    Article  CAS  PubMed  Google Scholar 

  48. Baur R, Beech R, Sigel E, Rufener L. Monepantel irreversibly binds to and opens Haemonchus contortus MPTL-1 and Caenorhabditis elegans ACR-20 receptors. Mol Pharmacol. 2015;87(1):96–102.

    Article  PubMed  CAS  Google Scholar 

  49. Bartley DJ, Devin L, Nath M, Morrison AA. Selection and characterisation of monepantel resistance in Teladorsagia circumcincta isolates. Int J Parasitol Drugs Drug Resist. 2015;5(2):69–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Scott I, Pomroy WE, Kenyon PR, Smith G, Adlington B, Moss A. Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Vet Parasitol. 2013;198(1–2):166–71.

    Article  CAS  PubMed  Google Scholar 

  51. Van den Brom R, Moll L, Kappert C, Vellema P. Haemonchus contortus resistance to monepantel in sheep. Vet Parasitol. 2015;209(3–4):278–80.

    Article  PubMed  CAS  Google Scholar 

  52. Čolović MB, Krstić DZ, Lazarević-Pašti TD, Bondžić AM, Vasić VM. Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol. 2013;11(3):315–35.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Fiel C, Guzmán M, Steffan P, Rodriguez E, Prieto O, Bhushan C. The efficacy of trichlorphon and naphthalophos against multiple anthelmintic-resistant nematodes of naturally infected sheep in Argentina. Parasitol Res. 2011;109(1):139–48.

    Article  Google Scholar 

  54. Le Jambre LF, Barger IA. Efficiency of rafoxanide and naphthalophos against inhibited Haemonchus contortus. Aust Vet J. 1979;55(7):346–7.

    Article  PubMed  Google Scholar 

  55. Green PE, Forsyth BA, Rowan KJ, Payne G. The isolation of a field strain of Haemonchus contortus in Queensland showing multiple anthelmintic resistance. Aust Vet J. 1981;57(2):79–84.

    Article  CAS  PubMed  Google Scholar 

  56. Swan GE. The pharmacology of halogenated salicylanilides and their anthelmintic use in animals. J S Afr Vet Assoc. 1999;70(2):61–70.

    CAS  PubMed  Google Scholar 

  57. Mohammed-Ali NA, Bogan JA. The pharmacodynamics of the flukicidal salicylanilides, rafoxanide, closantel and oxyclosanide. J Vet Pharmacol Ther. 1987;10(2):127–33.

    Article  CAS  PubMed  Google Scholar 

  58. Hall CA, Kelly JD, Whitlock HV, Ritchie L. Prolonged anthelmintic effect of closantel and disophenol against a thiabendazole selected resistant strain of Haemonchus contortus in sheep. Res Vet Sci. 1981;31(1):104–6.

    CAS  PubMed  Google Scholar 

  59. Australasian Animal Parasites Inside and Out. Australian Society for Parastology. 2015. http://parasite.org.au/publications/australian-animal-parasites-inside-and-out/

  60. Taylor A, Coop RL, Wall RL. Veterinary parasitology. Chichester: Wiley; 2013.

    Google Scholar 

  61. Kane HJ, Behm CA, Bryant C. Metabolic studies on the new fasciolicidal drug, closantel. Mol Biochem Parasitol. 1980;1(6):347–55.

    Article  CAS  PubMed  Google Scholar 

  62. van der Lugt JJ, Venter I. Myelin vacuolation, optic neuropathy and retinal degeneration after closantel overdosage in sheep and in a goat. J Comp Pathol. 2007;136(2–3):87–95.

    Article  PubMed  CAS  Google Scholar 

  63. Bennett JL, Kohler P. Fasciola hepatica: action in vitro of triclabendazole on immature and adult stages. Exp Parasitol. 1987;63(1):49–57.

    Article  CAS  PubMed  Google Scholar 

  64. Boray JC, Crowfoot PD, Strong MB, Allison JR, Schellenbaum M, Von Orelli M, et al. Treatment of immature and mature Fasciola hepatica infections in sheep with triclabendazole. Vet Rec. 1983;113(14):315–7.

    Article  CAS  PubMed  Google Scholar 

  65. Fairweather I. Triclabendazole: new skills to unravel an old(ish) enigma. J Helminthol. 2005;79(3):227–34.

    Article  CAS  PubMed  Google Scholar 

  66. Hennessy DR, Lacey E, Steel JW, Prichard RK. The kinetics of triclabendazole disposition in sheep. J Vet Pharmacol Ther. 1987;10(1):64–72.

    Article  CAS  PubMed  Google Scholar 

  67. Fairweather I, Boray J. Fasciolicides: efficacy, actions, resistance and its management. Vet J. 1999;158(2):81–112.

    Article  CAS  PubMed  Google Scholar 

  68. Savage J, Meaney M, Brennan GP, Hoey E, Trudgett A, Fairweather I. Disruption of vitellogenesis and spermatogenesis by triclabendazole (TCBZ) in a TCBZ-resistant isolate of Fasciola hepatica following incubation in vitro with a P-glycoprotein inhibitor. Parasitology. 2014;141(8):1064–79.

    Article  CAS  PubMed  Google Scholar 

  69. Little PR, Hodge A, Maeder SJ, Wirtherle NC, Nicholas DR, Cox GG, et al. Efficacy of a combined oral formulation of derquantel–abamectin against the adult and larval stages of nematodes in sheep, including anthelmintic-resistant strains. Vet Parasitol. 2011;181(2–4):180–93.

    Article  CAS  PubMed  Google Scholar 

  70. Epe C, Kaminsky R. New advancement in anthelmintic drugs in veterinary medicine. Trends Parasitol. 2013;29(3):129–34.

    Article  CAS  PubMed  Google Scholar 

  71. George SD, George AJ, Stein PA, Rolfe PF, Hosking BC, Seewald W. The comparative efficacy of abamectin, monepantel and an abamectin/derquantel combination against fourth-stage larvae of a macrocyclic lactone-resistant Teladorsagia spp. isolate infecting sheep. Vet Parasitol. 2012;188(1–2):190–3.

    Article  CAS  PubMed  Google Scholar 

  72. Geurden T, Hodge A, Noé L, Winstanley D, Bartley DJ, Taylor M, et al. The efficacy of a combined oral formulation of derquantel–abamectin against anthelmintic resistant gastro-intestinal nematodes of sheep in the UK. Vet Parasitol. 2012;189(2–4):308–16.

    Article  CAS  PubMed  Google Scholar 

  73. Kaminsky R, Bapst B, Stein PA, Strehlau GA, Allan BA, Hosking BC, et al. Differences in efficacy of monepantel, derquantel and abamectin against multi-resistant nematodes of sheep. Parasitol Res. 2011;109(1):19–23.

    Article  PubMed  Google Scholar 

  74. Ruiz-Lancheros E, Viau C, Walter TN, Francis A, Geary TG. Activity of novel nicotinic anthelmintics in cut preparations of Caenorhabditis elegans. Int J Parasitol. 2011;41(3–4):455–61.

    Article  CAS  PubMed  Google Scholar 

  75. Martin RJ, Puttachary S, Buxton SK, Verma S, Robertson AP. The Conqueror Worm: recent advances with cholinergic anthelmintics and techniques excite research for better therapeutic drugs. J Helminthol. 2015;89(4):387–97.

    Article  CAS  PubMed  Google Scholar 

  76. Prichard RK, Hall CA, Kelly JD, Martin ICA, Donald AD. The problem of anthelmintic resistance in nematodes. Aust Vet J. 1980;56(5):239–50.

    Article  CAS  PubMed  Google Scholar 

  77. Sutherland I, Scott I. Gastrointestinal nematodes of sheep and cattle: biology and control. London: Wiley; 2009.

    Google Scholar 

  78. Jackson F, Coop RL. The development of anthelmintic resistance in sheep nematodes. Parasitology. 2000;120(Suppl):S95–107.

    Article  PubMed  Google Scholar 

  79. Sutherst RW, Comins HN. The management of acaricide resistance in the cattle tick, Boophilus microplus (Canestrini) (Acari: Ixodidae), in Australia. Bull Entomol Res. 1979;69(3):519–37.

    Article  Google Scholar 

  80. Jackson R, Rhodes AP, Pomroy WE, Leathwick DM, West DM, Waghorn TS, et al. Anthelmintic resistance and management of nematode parasites on beef cattle-rearing farms in the North Island of New Zealand. N Z Vet J. 2006;54(6):289–96.

    Article  CAS  PubMed  Google Scholar 

  81. Molento MB. Parasite control in the age of drug resistance and changing agricultural practices. Vet Parasitol. 2009;163(3):229–34.

    Article  PubMed  Google Scholar 

  82. Woodgate RG, Besier RB. Sustainable use of anthelmintics in an integrated parasite management program for sheep nematodes. Anim Prod Sci. 2010;50(6):440–3.

    Article  Google Scholar 

  83. Nielsen MK. Sustainable equine parasite control: perspectives and research needs. Vet Parasitol. 2012;185(1):32–44.

    Article  CAS  PubMed  Google Scholar 

  84. Lanusse C, Alvarez L, Lifschitz A. Pharmacological knowledge and sustainable anthelmintic therapy in ruminants. Vet Parasitol. 2014;204(1–2):18–33.

    Article  CAS  PubMed  Google Scholar 

  85. Leathwick DM, Besier RB. The management of anthelmintic resistance in grazing ruminants in Australasia—strategies and experiences. Vet Parasitol. 2014;204(1–2):44–54.

    Article  CAS  PubMed  Google Scholar 

  86. Martin PJ. Development and control of resistance to anthelmintics. Int J Parasitol. 1987;17(2):493–501.

    Article  CAS  PubMed  Google Scholar 

  87. Smith G, Grenfell BT, Isham V, Cornell S. Anthelmintic resistance revisited: under-dosing, chemoprophylactic strategies, and mating probabilities. Int J Parasitol. 1999;29(1):77–91.

    Article  CAS  PubMed  Google Scholar 

  88. Besier RB, Hopkins DL. Anthelmintic dose selection by farmers. Aust Vet J. 1988;65(6):193–4.

    Article  CAS  PubMed  Google Scholar 

  89. Coles GC. Nematode control practices and anthelmintic resistance on British sheep farms. Vet Rec. 1997;141(4):91–3.

    Article  CAS  PubMed  Google Scholar 

  90. McMahon C, McCoy M, Ellison SE, Barley JP, Edgar HW, Hanna RE, et al. Anthelmintic resistance in Northern Ireland (III): uptake of 'SCOPS' (Sustainable Control of Parasites in Sheep) recommendations by sheep farmers. Vet Parasitol. 2013;193(1-3):179–84.

    Article  CAS  PubMed  Google Scholar 

  91. Nielsen MK, Fritzen B, Duncan JL, Guillot J, Eysker M, Dorchies P, et al. Practical aspects of equine parasite control: a review based upon a workshop discussion consensus. Equine Vet J. 2010;42(5):460–8.

    Article  CAS  PubMed  Google Scholar 

  92. Martin PJ, Anderson N, Jarrett RG, Brown TH, Ford GE. Effects of a preventive and suppressive control scheme on the development of thiabendazole-resistance in Ostertagia spp. Aust Vet J. 1982;58(5):185–90.

    Article  CAS  PubMed  Google Scholar 

  93. Barton NJ. Development of anthelmintic resistance in nematodes from sheep in Australia subjected to different treatment frequencies. Int J Parasitol. 1983;13(2):125–32.

    Article  CAS  PubMed  Google Scholar 

  94. Edwards JR, Wroth R, de Chaneet GC, Besier RB, Karlsson J, Morcombe PW, et al. Survey of anthelmintic resistance in Western Australian sheep flocks 2. Relationship with sheep management and parasite control practices. Aust Vet J. 1986;63(5):139–44.

    Article  CAS  PubMed  Google Scholar 

  95. Chartier C, Pors I, Hubert J, Rocheteau D, Benoit C, Bernard N. Prevalence of anthelmintic resistant nematodes in sheep and goats in Western France. Small Rumin Res. 1998;29(1):33–41.

    Article  Google Scholar 

  96. Chandrawathani P, Adnan M, Waller PJ. Anthelmintic resistance in sheep and goat farms on Peninsular Malaysia. Vet Parasitol. 1999;82(4):305–10.

    Article  CAS  PubMed  Google Scholar 

  97. Nielsen MK, Kaplan RM, Thamsborg SM, Monrad J, Olsen SN. Climatic influences on development and survival of free-living stages of equine strongyles: Implications for worm control strategies and managing anthelmintic resistance. Vet J. 2007;174(1):23–32.

    Article  PubMed  Google Scholar 

  98. Relf VE, Morgan ER, Hodgkinson JE, Matthews JB. A questionnaire study on parasite control practices on UK breeding Thoroughbred studs. Equine Vet J. 2012;44(4):466–71.

    Article  CAS  PubMed  Google Scholar 

  99. Prichard RK, Hennessy DR, Steel JW. Prolonged administration: a new concept for increasing the spectrum and effectiveness of anthelmintics. Vet Parasitol. 1978;4(4):309–15.

    Article  CAS  Google Scholar 

  100. Kelly JD, Hall CA, Whitlock HV, Thompson HG, Campbell NJ, Martin IC. The effect of route of administration on the anthelmintic efficacy of benzimidazole anthelmintics in sheep infected with strains of Haemonchus contortus and Trichostrongylus colubriformis resistant or susceptible to thiabendazole. Res Vet Sci. 1977;22(2):161–8.

    CAS  PubMed  Google Scholar 

  101. Hennessy DR. Modifying the formulation or delivery mechanism to increase the activity of anthelmintic compounds. Vet Parasitol. 1997;72(3–4):367–90.

    Article  CAS  PubMed  Google Scholar 

  102. Sargison N, Pomroy W, Adlington B. Ruminoreticulum bypass in goats and its possible effect on the efficacy of oxfendazole against resistant gastrointestinal parasites. Small Rumin Res. 2000;35(3):209–12.

    Article  Google Scholar 

  103. Borgsteede FHM. The efficacy and persistent anthelmintic effect of ivermectin in sheep. Vet Parasitol. 1993;50(1–2):117–24.

    Article  CAS  PubMed  Google Scholar 

  104. Gopal R, West D, Pomroy W. The difference in efficacy of ivermectin oral, moxidectin oral and moxidectin injectable formulations against an ivermectin-resistant strain of Trichostrongylus colubriformis in sheep. N Z Vet J. 2001;49(4):133–7.

    Article  CAS  PubMed  Google Scholar 

  105. Alka GRM, Sandhu KS, Sidhu PK. Efficacy of abamectin against ivermectin-resistant strain of Trichostrongylus colubriformis in sheep. Vet Parasitol. 2004;121(3–4):277–83.

    Article  CAS  PubMed  Google Scholar 

  106. Leathwick D, Miller C. Efficacy of oral, injectable and pour-on formulations of moxidectin against gastrointestinal nematodes in cattle in New Zealand. Vet Parasitol. 2013;191(3):293–300.

    Article  CAS  PubMed  Google Scholar 

  107. Areskog M, Ljungström B, Höglund J. Limited efficacy of pour-on anthelmintic treatment of cattle under Swedish field conditions. Int J Parasitol Drugs Drug Resist. 2013;3:129–34.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Sallovitz JM, Lifschitz A, Imperiale F, Virkel G, Larghi J, Lanusse C. Doramectin concentration profiles in the gastrointestinal tract of topically-treated calves: Influence of animal licking restriction. Vet Parasitol. 2005;133(1):61–70.

    Article  CAS  PubMed  Google Scholar 

  109. Gogolewski RP, Slacek B, Familton AS, Paterson B, Langholff WK, Allerton GR, et al. Efficacy of a topical formulation of eprinomectin against endoparasites of cattle in New Zealand. N Z Vet J. 1997;45(1):1–3.

    Article  CAS  PubMed  Google Scholar 

  110. Bousquet-Melou A, Mercadier S, Alvinerie M, Toutain PL. Endectocide exchanges between grazing cattle after pour-on administration of doramectin, ivermectin and moxidectin. Int J Parasitol. 2004;34(11):1299–307.

    Article  CAS  PubMed  Google Scholar 

  111. Sargent RM, Chambers M, Elliott T. Seasonal differences in the efficacy of pour-on formulations of triclabendazole and ivermectin or abamectin against late immature liver fluke (Fasciola hepatica) in cattle. Vet Parasitol. 2009;161(1–2):133–7.

    Article  CAS  PubMed  Google Scholar 

  112. Toutain PL, Modric S, Bousquet-MÉLou A, Sallovitz JM, Lanusse C. Should licking behavior be considered in the bioavailability evaluation of transdermal products? J Vet Pharmacol Ther. 2012;35:39–43.

    Article  PubMed  Google Scholar 

  113. Chartier C, Pors I, Bernard N, Hubert J. Efficacy of an albendazole slow-release capsule for the control of susceptible or resistant nematode parasites of dairy goats. Vet Parasitol. 1996;67(3–4):197–206.

    Article  CAS  PubMed  Google Scholar 

  114. Dobson RJ, Lejambre L, Gill JH. Management of anthelmintic resistance: Inheritance of resistance and selection with persistent drugs. Int J Parasitol. 1996;26(8–9):993–1000.

    Article  CAS  PubMed  Google Scholar 

  115. Dobson RJ, Besier RB, Barnes EH, Love SCJ, Vizard A, Bell K, et al. Principles for the use of macrocyclic lactones to minimise selection for resistance. Aust Vet J. 2001;79(11):756–61.

    Article  CAS  PubMed  Google Scholar 

  116. Lawrence KE, Rhodes AP, Jackson R, Leathwick DM, Heuer C, Pomroy WE, et al. Farm management practices associated with macrocyclic lactone resistance on sheep farms in New Zealand. N Z Vet J. 2006;54(6):283–8.

    Article  CAS  PubMed  Google Scholar 

  117. Leathwick DM, Hosking BC, Bisset SA, McKay CH. Managing anthelmintic resistance: Is it feasible in New Zealand to delay the emergence of resistance to a new anthelmintic class? N Z Vet J. 2009;57(4):181–92.

    Article  CAS  PubMed  Google Scholar 

  118. Ali DN, Hennessy DR. The effect of level of feed intake on the pharmacokinetic disposition and efficacy of ivermectin in sheep. J Vet Pharmacol Ther. 1996;19(2):89–94.

    Article  CAS  PubMed  Google Scholar 

  119. Hennessy D, Ali D. The effect of feed intake level on the pharmacokinetic disposition of closantel in sheep. Int J Parasitol. 1997;27(9):1081–6.

    Article  CAS  PubMed  Google Scholar 

  120. Anderson N, Martin PJ, Jarrett RG. Mixtures of anthelmintics: a strategy against resistance. Aust Vet J. 1988;65(2):62–4.

    Article  CAS  PubMed  Google Scholar 

  121. Anderson N, Martin PJ, Jarrett RG. Field evaluation of a mixture of albendazole sulphoxide and levamisole against Ostertagia and Trichostrongylus spp. in sheep. Aust Vet J. 1991;68(4):133–6.

    Article  CAS  PubMed  Google Scholar 

  122. Anderson N, Martin PJ, Jarrett RG. The efficacy of mixtures of albendazole sulphoxide and levamisole against sheep nematodes resistant to benzimidazole and levamisole. Aust Vet J. 1991;68(4):127–32.

    Article  CAS  PubMed  Google Scholar 

  123. Smith G. A mathematical model for the evolutions of anthelmintic resistance in a direct life cycle nematode parasite. Int J Parasitol. 1990;20(7):913–21.

    Article  CAS  PubMed  Google Scholar 

  124. Waller PJ, Dobson RJ, Haughey KG. The effect of combinations of anthelmintics on parasite populations in sheep. Aust Vet J. 1990;67(4):138–40.

    Article  CAS  PubMed  Google Scholar 

  125. Barnes EH, Dobson RJ, Barger IA. Worm control and anthelmintic resistance: adventures with a model. Parasitol Today. 1995;11(2):56–63.

    Article  CAS  PubMed  Google Scholar 

  126. Geary TG, Hosking BC, Skuce PJ, von Samson-Himmelstjerna G, Maeder S, Holdsworth P, et al. World Association for the Advancement of Veterinary Parasitology (WAAVP) Guideline: Anthelmintic combination products targeting nematode infections of ruminants and horses. Vet Parasitol. 2012;190(1):306–16.

    Article  Google Scholar 

  127. Bartram DJ, Leathwick DM, Taylor MA, Geurden T, Maeder SJ. The role of combination anthelmintic formulations in the sustainable control of sheep nematodes. Vet Parasitol. 2012;186(3–4):151–8.

    Article  CAS  PubMed  Google Scholar 

  128. Leathwick DM. Modelling the benefits of a new class of anthelmintic in combination. Vet Parasitol. 2012;186(1–2):93–100.

    Article  CAS  PubMed  Google Scholar 

  129. Leathwick DM, Waghorn TS, Miller CM, Candy PM, Oliver AMB. Managing anthelmintic resistance—use of a combination anthelmintic and leaving some lambs untreated to slow the development of resistance to ivermectin. Vet Parasitol. 2012;187(1–2):285–94.

    Article  CAS  PubMed  Google Scholar 

  130. Bartram DJ, Noé L, Krautmann MJ, Lane S, Geurden T. Clinical safety of rapid sequential administration of moxidectin injection and oral derquantel-abamectin as a quarantine treatment for introduced sheep. Vet Rec. 2013;172(16):426–7.

    Article  CAS  PubMed  Google Scholar 

  131. Leathwick DM, Ganesh S, Waghorn TS. Evidence for reversion towards anthelmintic susceptibility in Teladorsagia circumcincta in response to resistance management programmes. Int J Parasitol Drugs Drug Resist. 2015;5(1):9–15.

    Article  PubMed  PubMed Central  Google Scholar 

  132. McKenna PB. Update on the prevalence of anthelmintic resistance in gastrointestinal nematodes of sheep in New Zealand. N Z Vet J. 2010;58(3):172–3.

    Article  CAS  PubMed  Google Scholar 

  133. Puttachary S, Trailovic SM, Robertson AP, Thompson DP, Woods DJ, Martin RJ. Derquantel and abamectin: effects and interactions on isolated tissues of Ascaris suum. Mol Biochem Parasitol. 2013;188(2):79–86.

    Article  CAS  PubMed  Google Scholar 

  134. Walker RS, Miller JE, Monlezun CJ, LaMay D, Navarre C, Ensley D. Gastrointestinal nematode infection and performance of weaned stocker calves in response to anthelmintic control strategies. Vet Parasitol. 2013;197(1–2):152–9.

    Article  CAS  PubMed  Google Scholar 

  135. Smith LL. Combination anthelmintics effectively control ML-resistant parasites; a real-world case history. Vet Parasitol. 2014;204(1–2):12–7.

    Article  CAS  PubMed  Google Scholar 

  136. Bennet E-M, Behm C, Bryant C, Chevis RAF. Synergistic action of mebendazole and levamisole in the treatment of a benzimidazole-resistant Haemonchus contortus in sheep. Vet Parasitol. 1980;7(3):207–14.

    Article  CAS  Google Scholar 

  137. Dobson RJ, Hosking BC, Besier RB, Love S, Larsen JW, Rolfe PF, et al. Minimising the development of anthelmintic resistance, and optimising the use of the novel anthelmintic monepantel, for the sustainable control of nematode parasites in Australian sheep grazing systems. Aust Vet J. 2011;89(5):160–6.

    Article  CAS  PubMed  Google Scholar 

  138. Suter RJ, Besier RB, Perkins NR, Robertson ID, Chapman HM. Sheep-farm risk factors for ivermectin resistance in Ostertagia circumcincta in Western Australia. Prev Vet Med. 2004;63(3-4):257–69.

    Article  CAS  PubMed  Google Scholar 

  139. Michel JF. Strategies for the use of anthelmintics in livestock and their implications for the development of drug resistance. Parasitology. 1985;90(Pt 4):621–8.

    Article  PubMed  Google Scholar 

  140. Martin PJ, Anderson N, Jarrett RG. Detecting benzimidazole resistance with faecal egg count reduction tests and in vitro assays. Aust Vet J. 1989;66(8):236–40.

    Article  CAS  PubMed  Google Scholar 

  141. Gaba S, Cabaret J, Ginot V, Silvestre A. The early drug selection of nematodes to anthelmintics: stochastic transmission and population in refuge. Parasitology. 2006;133(Pt 3):345–56.

    Article  CAS  PubMed  Google Scholar 

  142. van Wyk JA. Refugia—overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort J Vet Res. 2001;68(1):55–67.

    PubMed  Google Scholar 

  143. Sissay MM, Asefa A, Uggla A, Waller PJ. Anthelmintic resistance of nematode parasites of small ruminants in eastern Ethiopia: exploitation of refugia to restore anthelmintic efficacy. Vet Parasitol. 2006;135(3–4):337–46.

    Article  CAS  PubMed  Google Scholar 

  144. Hughes PL, Dowling AF, Callinan AP. Resistance to macrocyclic lactone anthelmintics and associated risk factors on sheep farms in the lower North Island of New Zealand. N Z Vet J. 2007;55(4):177–83.

    Article  CAS  PubMed  Google Scholar 

  145. Besier RB. Targeted treatment strategies for sustainable worm control in small ruminants. Trop Biomed. 2008;25(1 Suppl):9–17.

    CAS  PubMed  Google Scholar 

  146. Waghorn TS, Leathwick DM, Miller CM, Atkinson DS. Brave or gullible: testing the concept that leaving susceptible parasites in refugia will slow the development of anthelmintic resistance. N Z Vet J. 2008;56(4):158–63.

    Article  CAS  PubMed  Google Scholar 

  147. Kenyon F, Greer AW, Coles GC, Cringoli G, Papadopoulos E, Cabaret J, et al. The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants. Vet Parasitol. 2009;164(1):3–11.

    Article  CAS  PubMed  Google Scholar 

  148. Martin PJ, Le Jambre LF, Claxton JH. The impact of refugia on the development of thiabendazole resistance in Haemonchus contortus. Int J Parasitol. 1981;11(1):35–41.

    Article  CAS  PubMed  Google Scholar 

  149. Leathwick DM, Miller CM, Atkinson DS, Haack NA, Alexander RA, Oliver AM, et al. Drenching adult ewes: implications of anthelmintic treatments pre- and post-lambing on the development of anthelmintic resistance. N Z Vet J. 2006;54(6):297–304.

    Article  CAS  PubMed  Google Scholar 

  150. Leathwick DM, Waghorn TS, Miller CM, Atkinson DS, Haack NA, Oliver AM. Selective and on-demand drenching of lambs: impact on parasite populations and performance of lambs. N Z Vet J. 2006;54(6):305–12.

    Article  CAS  PubMed  Google Scholar 

  151. Woodgate RG, Love S. WormKill to WormBoss—can we sell sustainable sheep worm control? Vet Parasitol. 2012;186(1–2):51–7.

    Article  CAS  PubMed  Google Scholar 

  152. Waghorn TS, Miller CM, Oliver AM, Leathwick DM. Drench-and-shift is a high-risk practice in the absence of refugia. N Z Vet J. 2009;57(6):359–63.

    Article  CAS  PubMed  Google Scholar 

  153. Van Wyk JA, Bath GF. The FAMACHA system for managing haemonchosis in sheep and goats by clinically identifying individual animals for treatment. Vet Res. 2002;33(5):509–29.

    Article  PubMed  Google Scholar 

  154. Leask R, Van Wyk JA, Thompson PN, Bath GF. The effect of application of the FAMACHA© system on selected production parameters in sheep. Small Rumin Res. 2013;110(1):1–8.

    Article  Google Scholar 

  155. Greer AW, Kenyon F, Bartley DJ, Jackson EB, Gordon Y, Donnan AA, et al. Development and field evaluation of a decision support model for anthelmintic treatments as part of a targeted selective treatment (TST) regime in lambs. Vet Parasitol. 2009;164(1):12–20.

    Article  CAS  PubMed  Google Scholar 

  156. Cornelius MP, Jacobson C, Besier RB. Body condition score as a selection tool for targeted selective treatment-based nematode control strategies in Merino ewes. Vet Parasitol. 2014;206(3–4):173–81.

    Article  CAS  PubMed  Google Scholar 

  157. O’Shaughnessy J, Earley B, Mee JF, Doherty ML, Crosson P, Barrett D, et al. Nematode control in spring-born suckler beef calves using targeted selective anthelmintic treatments. Vet Parasitol. 2014;205(1–2):150–7.

    Article  PubMed  Google Scholar 

  158. Lester HE, Bartley DJ, Morgan ER, Hodgkinson JE, Stratford CH, Matthews JB. A cost comparison of faecal egg count-directed anthelmintic delivery versus interval programme treatments in horses. Vet Rec. 2013;173(15):371–4.

    Article  CAS  PubMed  Google Scholar 

  159. Lester HE, Matthews JB. Faecal worm egg count analysis for targeting anthelmintic treatment in horses: points to consider. Equine Vet J. 2014;46(2):139–45.

    Article  CAS  PubMed  Google Scholar 

  160. Stafford KA, Morgan ER, Coles GC. Weight-based targeted selective treatment of gastrointestinal nematodes in a commercial sheep flock. Vet Parasitol. 2009;164(1):59–65.

    Article  CAS  PubMed  Google Scholar 

  161. Besier RB, Love RA, Lyon J, Van Burgel AJ. A targeted selective treatment approach for effective and sustainable sheep worm management: investigations in Western Australia. Anim Prod Sci. 2010;50(12):1034–42.

    Article  Google Scholar 

  162. Chylinski C, Cortet J, Neveu C, Cabaret J. Exploring the limitations of pathophysiological indicators used for targeted selective treatment in sheep experimentally infected with Haemonchus contortus. Vet Parasitol. 2015;207(1–2):85–93.

    Article  CAS  PubMed  Google Scholar 

  163. Leathwick DM, Miller CM, Atkinson DS, Haack NA, Waghorn TS, Oliver AM. Managing anthelmintic resistance: untreated adult ewes as a source of unselected parasites, and their role in reducing parasite populations. N Z Vet J. 2008;56(4):184–95.

    Article  CAS  PubMed  Google Scholar 

  164. Fairweather I. Raising the bar on reporting ‘triclabendazole resistance’. Vet Rec. 2011;168(19):514–5.

    Article  PubMed  Google Scholar 

  165. Gaasenbeek CPH, Moll L, Cornelissen JBWJ, Vellema P, Borgsteede FHM. An experimental study on triclabendazole resistance of Fasciola hepatica in sheep. Vet Parasitol. 2001;95(1):37–43.

    Article  CAS  PubMed  Google Scholar 

  166. Hennessy DR. The disposition of antiparasitic drugs in relation to the development of resistance by parasites of livestock. Acta Trop. 1994;56:125–41.

    Article  CAS  PubMed  Google Scholar 

  167. Matthews JB, Burden FA. Common helminth infections of donkeys and their control in temperate regions. Equine Vet Edu. 2013;25(9):461–7.

    Article  Google Scholar 

  168. Presidente P. Methods for detection of resistance to anthelmintics. In: Anderson N, Waller P, editors. Resistance in nematodes to anthelmintic drugs. Australia: CSIRO; 1985. p. 13–27.

    Google Scholar 

  169. Wood IB, Amaral NK, Bairden K, Duncan JL, Kassai T, Malone Jr JB, et al. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.): second edition of guidelines for evaluating the efficacy of anthelmintics in ruminants (bovine, ovine, caprine). Vet Parasitol. 1995;58(3):181–213.

    Article  CAS  PubMed  Google Scholar 

  170. Duncan JL, Abbott EM, Arundel JH, Eysker M, Klei TR, Krecek RC, et al. World Association for the Advancement of Veterinary Parasitology (WAAVP): second edition of guidelines for evaluating the efficacy of equine anthelmintics. Vet Parasitol. 2002;103(1–2):1–18.

    Article  CAS  PubMed  Google Scholar 

  171. Taylor MA, Hunt KR, Goodyear KL. Anthelmintic resistance detection methods. Vet Parasitol. 2002;103(3):183–94.

    Article  CAS  PubMed  Google Scholar 

  172. Vercruysse J, Holdsworth P, Letonja T, Conder G, Hamamoto K, Okano K, et al. International harmonisation of anthelmintic efficacy guidelines (Part 2). Vet Parasitol. 2002;103(4):277–97.

    Article  CAS  PubMed  Google Scholar 

  173. Ortiz P, Scarcella S, Cerna C, Rosales C, Cabrera M, Guzmán M, et al. Resistance of Fasciola hepatica against triclabendazole in cattle in Cajamarca (Peru): a clinical trial and an in vivo efficacy test in sheep. Vet Parasitol. 2013;195(1–2):118–21.

    Article  CAS  PubMed  Google Scholar 

  174. Sanabria R, Ceballos L, Moreno L, Romero J, Lanusse C, Alvarez L. Identification of a field isolate of Fasciola hepatica resistant to albendazole and susceptible to triclabendazole. Vet Parasitol. 2013;193(1):105–10.

    Article  CAS  PubMed  Google Scholar 

  175. Lyndal-Murphy M. Anthelmintic resistance in sheep. Australian standard diagnostic techniques for animal diseases. Australia: Standing Committee on Agriculture and Resource Management; 1992. p. 1–17.

    Google Scholar 

  176. Gordon D, Zadoks R, Skuce P, Sargison N. Confirmation of triclabendazole resistance in liver fluke in the UK. Vet Rec. 2012;171(6):159–60.

    Article  PubMed  Google Scholar 

  177. Gill JH, Redwin JM, Van WJA, Lacey E. Avermectin inhibition of larval development in Haemonchus contortus: effects of ivermectin resistance. Int J Parasitol. 1995;25(4):463–70.

    Article  CAS  PubMed  Google Scholar 

  178. Kelly JD, Sangster NC, Porter CJ. Use of guinea pigs to assay anthelmintic resistance in ovine isolates of Trichostrongylus colubriformis. Res Vet Sci. 1981;30:131–7.

    CAS  PubMed  Google Scholar 

  179. Conder GA, Thompson DP, Johnson SS. Demonstration of co-resistance of Haemonchus contortus to ivermectin and moxidectin. Vet Rec. 1993;132:651–2.

    Article  CAS  PubMed  Google Scholar 

  180. Kochapakdee S, Pandey VS, Pralomkarn W, Choldumrongkul S, Ngampongsai W, Lawpetchara A. Anthelmintic resistance in goats in southern Thailand. Vet Rec. 1995;137(5):124–5.

    Article  CAS  PubMed  Google Scholar 

  181. Coles G, Jackson F, Pomroy W, Prichard R, von Samson-Himmelstjerna G, Silvestre A, et al. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol. 2006;136(3):167–85.

    Article  CAS  PubMed  Google Scholar 

  182. McKenna PB. How do you mean? The case for composite faecal egg counts in testing for drench resistance. N Z Vet J. 2007;55(2):100–1.

    Article  CAS  PubMed  Google Scholar 

  183. Levecke B, Rinaldi L, Charlier J, Maurelli MP, Bosco A, Vercruysse J, et al. The bias, accuracy and precision of faecal egg count reduction test results in cattle using McMaster, Cornell-Wisconsin and FLOTAC egg counting methods. Vet Parasitol. 2012;188(1–2):194–9.

    Article  CAS  PubMed  Google Scholar 

  184. Calvete C, Uriarte J. Improving the detection of anthelmintic resistance: evaluation of faecal egg count reduction test procedures suitable for farm routines. Vet Parasitol. 2013;196(3–4):438–52.

    Article  PubMed  Google Scholar 

  185. McKenna PB. Are multiple pre-treatment groups necessary or unwarranted in faecal egg count reduction tests in sheep? Vet Parasitol. 2013;196(3–4):433–7.

    Article  CAS  PubMed  Google Scholar 

  186. Lyndal-Murphy M, Swain AJ, Pepper PM. Methods to determine resistance to anthelmintics when continuing larval development occurs. Vet Parasitol. 2014;199(3–4):191–200.

    Article  CAS  PubMed  Google Scholar 

  187. McKenna PB. Further studies on the necessity or otherwise of multiple pre-treatment groups in faecal egg count reduction tests in sheep. Vet Parasitol. 2014;200(1–2):212–5.

    Article  CAS  PubMed  Google Scholar 

  188. Rinaldi L, Levecke B, Bosco A, Ianniello D, Pepe P, Charlier J, et al. Comparison of individual and pooled faecal samples in sheep for the assessment of gastrointestinal strongyle infection intensity and anthelmintic drug efficacy using McMaster and Mini-FLOTAC. Vet Parasitol. 2014;205(1-2):216–23.

    Article  CAS  PubMed  Google Scholar 

  189. Coles GC, Bauer C, Borgsteede FHM, Geerts S, Klei TR, Taylor MA, et al. 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(1–2):35–44.

    Article  CAS  PubMed  Google Scholar 

  190. Demeler J, Schein E, von Samson-Himmelstjerna G. Advances in laboratory diagnosis of parasitic infections of sheep. Vet Parasitol. 2012;189(1):52–64.

    Article  CAS  PubMed  Google Scholar 

  191. Cabaret J, Berrag B. Faecal egg count reduction test for assessing anthelmintic efficacy: average versus individually based estimations. Vet Parasitol. 2004;121(1–2):105–13.

    Article  CAS  PubMed  Google Scholar 

  192. Morgan ER, Cavill L, Curry GE, Wood RM, Mitchell ES. Effects of aggregation and sample size on composite faecal egg counts in sheep. Vet Parasitol. 2005;131(1–2):79–87.

    Article  CAS  PubMed  Google Scholar 

  193. Dobson RJ, Sangster NC, Besier RB, Woodgate RG. Geometric means provide a biased efficacy result when conducting a faecal egg count reduction test (FECRT). Vet Parasitol. 2009;161(1–2):162–7.

    Article  CAS  PubMed  Google Scholar 

  194. Dobson RJ, Hosking BC, Jacobson CL, Cotter JL, Besier RB, Stein PA, et al. Preserving new anthelmintics: a simple method for estimating faecal egg count reduction test (FECRT) confidence limits when efficacy and/or nematode aggregation is high. Vet Parasitol. 2012;186(1–2):79–92.

    Article  CAS  PubMed  Google Scholar 

  195. McKenna PB. Criteria for diagnosing anthelmintic resistance by the faecal egg count reduction test. N Z Vet J. 1994;42(4):153–4.

    Article  CAS  PubMed  Google Scholar 

  196. McKenna PB. Further potential limitations of the undifferentiated faecal egg count reduction test for the detection of anthelmintic resistance in sheep. N Z Vet J. 1997;45(6):244–6.

    Article  CAS  PubMed  Google Scholar 

  197. Webb RF, McCully CH, Adams BS. The efficiency of oxfendazole against four field populations of benzimidazole resistant Haemonchus contortus. Aust Vet J. 1979;55(5):249–50.

    CAS  PubMed  Google Scholar 

  198. Rinaldi L, Coles GC, Maurelli MP, Musella V, Cringoli G. Calibration and diagnostic accuracy of simple flotation, McMaster and FLOTAC for parasite egg counts in sheep. Vet Parasitol. 2011;177(3–4):345–52.

    Article  CAS  PubMed  Google Scholar 

  199. Working Party for the Animal Health Committee of the Standing Committee on Agriculture. Anthelmintic resistance. Melbourne: CSIRO; 1989.

    Google Scholar 

  200. Torgerson PR, Paul M, Furrer R. Evaluating faecal egg count reduction using a specifically designed package “eggCounts” in R and a user friendly web interface. Int J Parasitol. 2014;44(5):299–303.

    Article  PubMed  Google Scholar 

  201. McKenna PB. The detection of anthelmintic resistance by the faecal egg count reduction test: an examination of some of the factors affecting performance and interpretation. N Z Vet J. 1990;38(4):142–7.

    Article  CAS  PubMed  Google Scholar 

  202. Pomroy WE, Whelan N, Alexander AM, West DW, Stafford K, Adlington BA, et al. Multiple resistance in goat-derived Ostertagia and the efficacy of moxidectin and combinations of other anthelmintics. N Z Vet J. 1992;40(2):76–8.

    Article  CAS  PubMed  Google Scholar 

  203. Van Wyk JA, van Schalkwyk PC. A novel approach to the control of anthelmintic-resistant Haemonchus contortus in sheep. Vet Parasitol. 1990;35(1–2):61–9.

    PubMed  Google Scholar 

  204. Bird J, Shulaw WP, Pope WF, Bremer CA. Control of anthelmintic resistant endoparasites in a commercial sheep flock through parasite community replacement. Vet Parasitol. 2001;97(3):219–25.

    Article  CAS  PubMed  Google Scholar 

  205. Demeler J, Van Zeveren AMJ, Kleinschmidt N, Vercruysse J, Höglund J, Koopmann R, et al. Monitoring the efficacy of ivermectin and albendazole against gastro intestinal nematodes of cattle in Northern Europe. Vet Parasitol. 2009;160(1–2):109–15.

    Article  CAS  PubMed  Google Scholar 

  206. Edmonds MD, Johnson EG, Edmonds JD. Anthelmintic resistance of Ostertagia ostertagi and Cooperia oncophora to macrocyclic lactones in cattle from the western United States. Vet Parasitol. 2010;170(3–4):224–9.

    Article  CAS  PubMed  Google Scholar 

  207. El-Abdellati A, Geldhof P, Claerebout E, Vercruysse J, Charlier J. Monitoring macrocyclic lactone resistance in Cooperia oncophora on a Belgian cattle farm during four consecutive years. Vet Parasitol. 2010;171(1–2):167–71.

    Article  CAS  PubMed  Google Scholar 

  208. Demeler J, Kleinschmidt N, Küttler U, Koopmann R, von Samson-Himmelstjerna G. Evaluation of the egg hatch assay and the larval migration inhibition assay to detect anthelmintic resistance in cattle parasitic nematodes on farms. Parasitol Int. 2012;61(4):614–8.

    Article  CAS  PubMed  Google Scholar 

  209. Yazwinski TA, Tucker CA, Wray E, Jones L, Reynolds J, Hornsby P, et al. Control trial and fecal egg count reduction test determinations of nematocidal efficacies of moxidectin and generic ivermectin in recently weaned, naturally infected calves. Vet Parasitol. 2013;195(1–2):95–101.

    Article  CAS  PubMed  Google Scholar 

  210. Gasbarre LC. Anthelmintic resistance in cattle nematodes in the US. Vet Parasitol. 2014;204(1–2):3–11.

    Article  CAS  PubMed  Google Scholar 

  211. Das Neves JH, Carvalho N, Rinaldi L, Cringoli G, Amarante AF. Diagnosis of anthelmintic resistance in cattle in Brazil: a comparison of different methodologies. Vet Parasitol. 2014;206(3–4):216–26.

    Article  PubMed  CAS  Google Scholar 

  212. Smith G, Grenfell BT, Anderson RM. The regulation of Ostertagia ostertagi populations in calves: density-dependent control of fecundity. Parasitology. 1987;95(Pt 2):373–88.

    Article  PubMed  Google Scholar 

  213. Condi GK, Soutello RGV, Amarante AFT. Moxidectin-resistant nematodes in cattle in Brazil. Vet Parasitol. 2009;161(3–4):213–7.

    Article  CAS  PubMed  Google Scholar 

  214. De Graef J, Sarre C, Mills BJ, Mahabir S, Casaert S, De Wilde N, et al. Assessing resistance against macrocyclic lactones in gastro-intestinal nematodes in cattle using the faecal egg count reduction test and the controlled efficacy test. Vet Parasitol. 2012;189(2–4):378–82.

    Article  PubMed  Google Scholar 

  215. Suarez VH, Cristel SL. Anthelmintic resistance in cattle nematode in the western Pampeana Region of Argentina. Vet Parasitol. 2007;144(1–2):111–7.

    Article  CAS  PubMed  Google Scholar 

  216. Pook JF, Power ML, Sangster NC, Hodgson JL, Hodgson DR. Evaluation of tests for anthelmintic resistance in cyathostomes. Vet Parasitol. 2002;106:331–43.

    Article  CAS  PubMed  Google Scholar 

  217. Lawson E, Burden F, Elsheikha HM. Pyrantel resistance in two herds of donkey in the UK. Vet Parasitol. 2015;207(3-4):346–9.

    Article  CAS  PubMed  Google Scholar 

  218. 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(4):281–8.

    Article  CAS  PubMed  Google Scholar 

  219. Stratford CH, McGorum BC, Pickles KJ, Matthews JB. An update on cyathostomins: Anthelmintic resistance and diagnostic tools. Equine Vet J. 2011;43:133–9.

    Article  Google Scholar 

  220. Vidyashankar AN, Hanlon BM, Kaplan RM. Statistical and biological considerations in evaluating drug efficacy in equine strongyle parasites using fecal egg count data. Vet Parasitol. 2012;185(1):45–56.

    Article  CAS  PubMed  Google Scholar 

  221. Matthews JB. Anthelmintic resistance in equine nematodes. Int J Parasitol Drugs Drug Resist. 2014;4(3):310–5.

    Article  PubMed  PubMed Central  Google Scholar 

  222. Bauer C, Merkt JC, Janke-Grimm G, Burger HJ. Prevalence and control of benzimidazole-resistant small strongyles on German thoroughbred studs. Vet Parasitol. 1986;21(3):189–203.

    Article  CAS  PubMed  Google Scholar 

  223. Denwood MJ, Reid SW, Love S, Nielsen MK, Matthews L, McKendrick IJ, et al. Comparison of three alternative methods for analysis of equine Faecal Egg Count Reduction Test data. Prev Vet Med. 2010;93(4):316–23.

    Article  CAS  PubMed  Google Scholar 

  224. Craven J, Bjorn H, Henriksen SA, Nansen P, Larsen M, Lendal S. Survey of anthelmintic resistance on Danish horse farms, using 5 different methods of calculating faecal egg count reduction. Equine Vet J. 1998;30(4):289–93.

    Article  CAS  PubMed  Google Scholar 

  225. Sangster NC, Gill J. Pharmacology of anthelmintic resistance. Parasitol Today. 1999;15(4):141–6.

    Article  CAS  PubMed  Google Scholar 

  226. Larsen ML, Ritz C, Petersen SL, Nielsen MK. Determination of ivermectin efficacy against cyathostomins and Parascaris equorum on horse farms using selective therapy. Vet J. 2011;188(1):44–7.

    Article  CAS  PubMed  Google Scholar 

  227. Geurden T, Hoste H, Jacquiet P, Traversa D, Sotiraki S, Frangipane di Regalbono A, et al. Anthelmintic resistance and multidrug resistance in sheep gastro-intestinal nematodes in France, Greece and Italy. Vet Parasitol. 2014;201(1–2):59–66.

    Article  CAS  PubMed  Google Scholar 

  228. von Samson-Himmelstjerna G, Fritzen B, Demeler J, Schurmann S, Rohn K, Schnieder T, et al. 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(1–2):74–80.

    Article  CAS  Google Scholar 

  229. Rossano MG, Smith AR, Lyons ET. Shortened strongyle-type egg reappearance periods in naturally infected horses treated with moxidectin and failure of a larvicidal dose of fenbendazole to reduce faecal egg counts. Vet Parasitol. 2010;173(3–4):349–52.

    Article  CAS  PubMed  Google Scholar 

  230. Lyons ET, Tolliver SC, Ionita M, Collins SS. Evaluation of parasiticidal activity of fenbendazole, ivermectin, oxibendazole, and pyrantel pamoate in horse foals with emphasis on ascarids (Parascaris equorum) in field studies on five farms in Central Kentucky in 2007. Parasitol Res. 2008;103(2):287–91.

    Article  CAS  PubMed  Google Scholar 

  231. Happich FA, Boray JC. Quantitative diagnosis of chronic fasciolosis. 1. Comparative studies on quantitative faecal examinations for chronic Fasciola hepatica infection in sheep. Aust Vet J. 1969;45(7):326–8.

    Article  CAS  PubMed  Google Scholar 

  232. Conceição MAP, Durão RM, Costa IH, da Costa JMC. Evaluation of a simple sedimentation method (modified McMaster) for diagnosis of bovine fascioliosis. Vet Parasitol. 2002;105(4):337–43.

    Article  PubMed  Google Scholar 

  233. Rapsch C, Schweizer G, Grimm F, Kohler L, Bauer C, Deplazes P, et al. Estimating the true prevalence of Fasciola hepatica in cattle slaughtered in Switzerland in the absence of an absolute diagnostic test. Int J Parasitol. 2006;36(10–11):1153–8.

    Article  CAS  PubMed  Google Scholar 

  234. Charlier J, De Meulemeester L, Claerebout E, Williams D, Vercruysse J. Qualitative and quantitative evaluation of coprological and serological techniques for the diagnosis of fasciolosis in cattle. Vet Parasitol. 2008;153(1–2):44–51.

    Article  PubMed  Google Scholar 

  235. Flanagan M, Edgar D, Gordon A, Hanna R, Brennan G, Fairweather I. Comparison of two assays, a faecal egg count reduction test (FECRT) and a coproantigen reduction test (CRT), for the diagnosis of resistance to triclabendazole in Fasciola hepatica in sheep. Vet Parasitol. 2011;176:170–6.

    Article  CAS  PubMed  Google Scholar 

  236. Sargison ND. Diagnosis of triclabendazole resistance in Fasciola hepatica. Vet Rec. 2012;171(6):151–2.

    Article  PubMed  Google Scholar 

  237. Hanna REB, McMahon C, Ellison S, Edgar HW, Kajugu PE, Gordon A, et al. Fasciola hepatica: A comparative survey of adult fluke resistance to triclabendazole, nitroxynil and closantel on selected upland and lowland sheep farms in Northern Ireland using faecal egg counting, coproantigen ELISA testing and fluke histology. Vet Parasitol. 2015;207(1–2):34–43.

    Article  CAS  PubMed  Google Scholar 

  238. Anderson N, Luong TT, Vo NG, Bui KL, Smooker PM, Spithill TW. The sensitivity and specificity of two methods for detecting Fasciola infections in cattle. Vet Parasitol. 1999;83(1):15–24.

    Article  CAS  PubMed  Google Scholar 

  239. Flanagan AM, Edgar HWJ, Forster F, Gordon A, Hanna REB, McCoy M, et al. Standardisation of a coproantigen reduction test (CRT) protocol for the diagnosis of resistance to triclabendazole in Fasciola hepatica. Vet Parasitol. 2011;176(1):34–42.

    Article  CAS  PubMed  Google Scholar 

  240. Daniel R, van Dijk J, Jenkins T, Akca A, Mearns R, Williams DJL. Composite faecal egg count reduction test to detect resistance to triclabendazole in Fasciola hepatica. Vet Rec. 2012;171(6):153–5.

    Article  CAS  PubMed  Google Scholar 

  241. Brockwell YM, Elliott TP, Anderson GR, Stanton R, Spithill TW, Sangster NC. Confirmation of Fasciola hepatica resistant to triclabendazole in naturally infected Australian beef and dairy cattle. Int J Parasitol Drugs Drug Resist. 2014;4(1):48–54.

    Article  PubMed  Google Scholar 

  242. Robles-Perez D, Martinez-Perez JM, Rojo-Vazquez FA, Martinez-Valladares M. The diagnosis of fasciolosis in feces of sheep by means of a PCR and its application in the detection of anthelmintic resistance in sheep flocks naturally infected. Vet Parasitol. 2013;197(1–2):277–82.

    Article  CAS  PubMed  Google Scholar 

  243. Le Jambre LF. Egg hatch as an in vitro assay of thiabendazole resistance in nematodes. Vet Parasitol. 1976;2(4):385–91.

    Article  Google Scholar 

  244. Maingi N, Bjorn H, Dangolla A. The relationship between faecal egg count reduction and the lethal dose 50% in the egg hatch assay and larval development assay. Vet Parasitol. 1998;77(2–3):133–45.

    Article  CAS  PubMed  Google Scholar 

  245. Varady M, Corba J. Comparison of six in vitro tests in determining benzimidazole and levamisole resistance in Haemonchus contortus and Ostertagia circumcincta of sheep. Vet Parasitol. 1999;80(3):239–49.

    Article  CAS  PubMed  Google Scholar 

  246. Varady M, Cudekova P, Corba J. In vitro detection of benzimidazole resistance in Haemonchus contortus: egg hatch test versus larval development test. Vet Parasitol. 2007;149(1–2):104–10.

    Article  CAS  PubMed  Google Scholar 

  247. Diez-Banos P, Pedreira J, Sanchez-Andrade R, Francisco I, Suarez JL, Diaz P, et al. Field evaluation for anthelmintic-resistant ovine gastrointestinal nematodes by in vitro and in vivo assays. J Parasitol. 2008;94(4):925–8.

    Article  CAS  PubMed  Google Scholar 

  248. von Samson-Himmelstjerna G, Walsh TK, Donnan AA, Carriere S, Jackson F, Skuce PJ, et al. Molecular detection of benzimidazole resistance in Haemonchus contortus using real-time PCR and pyrosequencing. Parasitology. 2009;136(3):349–58.

    Article  CAS  Google Scholar 

  249. Cudekova P, Varady M, Dolinska M, Konigova A. Phenotypic and genotypic characterisation of benzimidazole susceptible and resistant isolates of Haemonchus contortus. Vet Parasitol. 2010;172(1–2):155–9.

    Article  CAS  PubMed  Google Scholar 

  250. Calvete C, Calavia R, Ferrer LM, Ramos JJ, Lacasta D, Uriarte J. Management and environmental factors related to benzimidazole resistance in sheep nematodes in Northeast Spain. Vet Parasitol. 2012;184(2–4):193–203.

    Article  CAS  PubMed  Google Scholar 

  251. Rialch A, Vatsya S, Kumar RR. Detection of benzimidazole resistance in gastrointestinal nematodes of sheep and goats of sub-Himalayan region of northern India using different tests. Vet Parasitol. 2013;198(3–4):312–8.

    Article  CAS  PubMed  Google Scholar 

  252. Calvete C, Ferrer LM, Lacasta D, Calavia R, Ramos JJ, Ruiz-de-Arkaute M, et al. Variability of the egg hatch assay to survey benzimidazole resistance in nematodes of small ruminants under field conditions. Vet Parasitol. 2014;203(1–2):102–13.

    Article  CAS  PubMed  Google Scholar 

  253. von Samson-Himmelstjerna G, Coles GC, Jackson F, Bauer C, Borgsteede F, Cirak VY, et al. Standardization of the egg hatch test for the detection of benzimidazole resistance in parasitic nematodes. Parasitol Res. 2009;105(3):825–34.

    Article  Google Scholar 

  254. Ihler CF, Bjorn H. Use of two in vitro methods for the detection of benzimidazole resistance in equine small strongyles (Cyathostoma spp.). Vet Parasitol. 1996;65(1–2):117–25.

    Article  PubMed  Google Scholar 

  255. Whitlock HV, Sangster NC, Gunawan M, Porter CJ, Kelly JD. Trichostrongylus colubriformis and Ostertagia sp. resistant to levamisole, morantel tartrate and thiabendazole: isolation into pure strain and anthelmintic titration. Res Vet Sci. 1980;29(1):31–5.

    CAS  PubMed  Google Scholar 

  256. Craven J, Bjorn H, Barnes EH, Henriksen SA, 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(1):49–59.

    Article  CAS  PubMed  Google Scholar 

  257. von Samson-Himmelstjerna G, von Witzendorff C, Sievers G, Schnieder T. Comparative use of faecal egg count reduction test, egg hatch assay and beta-tubulin codon 200 genotyping in small strongyles (Cyathostominae) before and after benzimidazole treatment. Vet Parasitol. 2002;108(3):227–35.

    Article  Google Scholar 

  258. Matthews JB, McArthur C, Robinson A, Jackson F. The in vitro diagnosis of anthelmintic resistance in cyathostomins. Vet Parasitol. 2012;185(1):25–31.

    Article  CAS  PubMed  Google Scholar 

  259. Fairweather I, McShane DD, Shaw L, Ellison SE, O’Hagan NT, York EA, et al. Development of an egg hatch assay for the diagnosis of triclabendazole resistance in Fasciola hepatica: proof of concept. Vet Parasitol. 2012;183(3–4):249–59.

    Article  CAS  PubMed  Google Scholar 

  260. Canevari J, Ceballos L, Sanabria R, Romero J, Olaechea F, Ortiz P, et al. Testing albendazole resistance in Fasciola hepatica: validation of an egg hatch test with isolates from South America and the United Kingdom. J Helminthol. 2014;88(3):286–92.

    Article  CAS  PubMed  Google Scholar 

  261. Chryssafidis AL, Fu Y, De Waal T, Mulcahy G. Standardisation of egg-viability assays for Fasciola hepatica and Calicophoron daubneyi: a tool for evaluating new technologies of parasite control. Vet Parasitol. 2015;210(1–2):25–31.

    Article  PubMed  Google Scholar 

  262. Taylor MA. A larval development test for the detection of anthelmintic resistance in nematodes of sheep. Res Vet Sci. 1990;49(2):198–202.

    CAS  PubMed  Google Scholar 

  263. Amarante AF, Pomroy WE, Charleston WA, Leathwick DM, Tornero MT. Evaluation of a larval development assay for the detection of anthelmintic resistance in Ostertagia circumcincta. Int J Parasitol. 1997;27(3):305–11.

    Article  CAS  PubMed  Google Scholar 

  264. Besier R. Field application of the Drenchrite test. Reaching new heights. In: Proceedings of the Australian Sheep Veterinary Society, 1998. p. 21–5.

    Google Scholar 

  265. Terrill TH, Kaplan RM, Larsen M, Samples OM, Miller JE, Gelaye S. Anthelmintic resistance on goat farms in Georgia: efficacy of anthelmintics against gastrointestinal nematodes in two selected goat herds. Vet Parasitol. 2001;97(4):261–8.

    Article  CAS  PubMed  Google Scholar 

  266. Kotze AC, Dobson RJ, Tyrrell KL, Stein PA. High-level ivermectin resistance in a field isolate of Haemonchus contortus associated with a low level of resistance in the larval stage: implications for resistance detection. Vet Parasitol. 2002;108(3):255–63.

    Article  CAS  PubMed  Google Scholar 

  267. Kaplan RM, Vidyashankar AN, Howell SB, Neiss JM, Williamson LH, Terrill TH. A novel approach for combining the use of in vitro and in vivo data to measure and detect emerging moxidectin resistance in gastrointestinal nematodes of goats. Int J Parasitol. 2007;37(7):795–804.

    Article  CAS  PubMed  Google Scholar 

  268. Varady M, Corba J, Letkova V, Kovac G. Comparison of two versions of larval development test to detect anthelmintic resistance in Haemonchus contortus. Vet Parasitol. 2009;160(3–4):267–71.

    Article  PubMed  Google Scholar 

  269. Demeler J, Gill JH, von Samson-Himmelstjerna G, Sangster NC. The in vitro assay profile of macrocyclic lactone resistance in three species of sheep trichostrongyloids. Int J Parasitol Drugs Drug Resist. 2013;3:109–18.

    Article  PubMed  PubMed Central  Google Scholar 

  270. Dolinská M, Königová A, Letková V, Molnár L, Várady M. Detection of ivermectin resistance by a larval development test—back to the past or a step forward? Vet Parasitol. 2013;198(1–2):154–8.

    Article  PubMed  CAS  Google Scholar 

  271. Lacey E, Redwin JM, Gill JH, Demargheriti VM, Waller PJ. A larval development assay for the simultaneous detection of broad spectrum anthelmintic resistance. In: Boray JC, Martin PJ, Roush RT, editors. Resistance of parasites to antiparasitic drugs: round table conference: ICOPA VII, Paris, 1990. Rahway: MSD AGVET Division of Merck; 1990. p. 177–84.

    Google Scholar 

  272. Palmer D, Mitchell T, Lyon J, Besier R. Laboratory experiences with DrenchRite. In: Proceedings of the Australian Sheep Veterinary Society, 1998. p. 1–9.

    Google Scholar 

  273. Demeler J, Küttler U, von Samson-Himmelstjerna G. Adaptation and evaluation of three different in vitro tests for the detection of resistance to anthelmintics in gastro intestinal nematodes of cattle. Vet Parasitol. 2010;170(1–2):61–70.

    Article  CAS  PubMed  Google Scholar 

  274. Tandon R, Kaplan RM. Evaluation of a larval development assay (DrenchRite) for the detection of anthelmintic resistance in cyathostomin nematodes of horses. Vet Parasitol. 2004;121(1–2):125–42.

    Article  CAS  PubMed  Google Scholar 

  275. Lind EO, Uggla A, Waller P, Hoglund J. Larval development assay for detection of anthelmintic resistance in cyathostomins of Swedish horses. Vet Parasitol. 2005;128(3–4):261–9.

    Article  CAS  PubMed  Google Scholar 

  276. Rothwell JT, Sangster NC. An in vitro assay utilising parasitic larval Haemonchus contortus to detect resistance to closantel and other anthelmintics. Int J Parasitol. 1993;23(5):573–8.

    Article  CAS  PubMed  Google Scholar 

  277. Small AJ, Coles GC. Detection of anthelmintic resistance by culture in vitro of parasitic stages of ovine nematodes. Vet Parasitol. 1993;51(1-2):163–6.

    Article  CAS  PubMed  Google Scholar 

  278. Bennett JL, Pax RA. Micromotility meter: instrumentation to analyse helminth motility. Parasitol Today. 1987;3(5):159–60.

    Article  CAS  PubMed  Google Scholar 

  279. Folz SD, Pax RA, Thomas EM, Bennett JL, Lee BL, Conder GA. Detecting in vitro anthelmintic effects with a micromotility meter. Vet Parasitol. 1987;24(3–4):241–50.

    Article  CAS  PubMed  Google Scholar 

  280. Storey B, Marcellino C, Miller M, Maclean M, Mostafa E, Howell S, et al. Utilization of computer processed high definition video imaging for measuring motility of microscopic nematode stages on a quantitative scale: “The Worminator”. Int J Parasitol Drugs Drug Resist. 2014;4(3):233–43.

    Article  PubMed  PubMed Central  Google Scholar 

  281. Wagland BM, Jones WO, Hribar L, Bendixsen T, Emery DL. A new simplified assay for larval migration inhibition. Int J Parasitol. 1992;22(8):1183–5.

    Article  CAS  PubMed  Google Scholar 

  282. d'Assonville JA, Janovsky E, Verster A. In vitro screening of Haemonchus contortus third stage larvae for ivermectin resistance. Vet Parasitol. 1996;61(1–2):73–80.

    Article  PubMed  Google Scholar 

  283. Kotze AC, Le Jambre LF, O’Grady J. A modified larval migration assay for detection of resistance to macrocyclic lactones in Haemonchus contortus, and drug screening with Trichostrongylidae parasites. Vet Parasitol. 2006;137(3–4):294–305.

    Article  CAS  PubMed  Google Scholar 

  284. Almeida GD, Feliz DC, Heckler RP, Borges DG, Onizuka MK, Tavares LE, et al. Ivermectin and moxidectin resistance characterization by larval migration inhibition test in field isolates of Cooperia spp. in beef cattle, Mato Grosso do Sul, Brazil. Vet Parasitol. 2013;191(1-2):59–65.

    Article  CAS  PubMed  Google Scholar 

  285. Álvarez-Sánchez MA, Pérez-García J, Cruz-Rojo MA, Rojo-Vázquez FA. Real time PCR for the diagnosis of benzimidazole resistance in trichostrongylids of sheep. Vet Parasitol. 2005;129(3–4):291–8.

    Article  PubMed  CAS  Google Scholar 

  286. Bartley DJ, McAllister H, Bartley Y, Dupuy J, Menez C, Alvinerie M, et al. P-glycoprotein interfering agents potentiate ivermectin susceptibility in ivermectin sensitive and resistant isolates of Teladorsagia circumcincta and Haemonchus contortus. Parasitology. 2009;136(9):1081–8.

    Article  CAS  PubMed  Google Scholar 

  287. Sheriff JC, Kotze AC, Sangster NC, Martin RJ. Effects of macrocyclic lactone anthelmintics on feeding and pharyngeal pumping in Trichostrongylus colubriformis in vitro. Parasitology. 2002;125(5):477–84.

    Google Scholar 

  288. Barrère V, Keller K, von Samson-Himmelstjerna G, Prichard RK. Efficiency of a genetic test to detect benzimidazole resistant Haemonchus contortus nematodes in sheep farms in Quebec, Canada. Parasitol Int. 2013;62(5):464–70.

    Article  PubMed  Google Scholar 

  289. Kwa MS, Veenstra JG, Roos MH. Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype 1. Mol Biochem Parasitol. 1994;63(2):299–303.

    Google Scholar 

  290. Elard L, Humbert JF. Importance of the mutation of amino acid 200 of the isotype 1 beta-tubulin gene in the benzimidazole resistance of the small-ruminant parasite Teladorsagia circumcincta. Parasitol Res. 1999;85(6):452–6.

    Article  CAS  PubMed  Google Scholar 

  291. Silvestre A, Cabaret J. Mutation in position 167 of isotype 1 beta-tubulin gene of Trichostrongylid nematodes: role in benzimidazole resistance? Mol Biochem Parasitol. 2002;120(2):297–300.

    Article  CAS  PubMed  Google Scholar 

  292. Ghisi M, Kaminsky R, Maser P. Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Vet Parasitol. 2007;144(3–4):313–20.

    Article  CAS  PubMed  Google Scholar 

  293. Rufener L, Kaminsky R, Maser P. In vitro selection of Haemonchus contortus for benzimidazole resistance reveals a mutation at amino acid 198 of beta-tubulin. Mol Biochem Parasitol. 2009;168(1):120–2.

    Article  CAS  PubMed  Google Scholar 

  294. Kotze AC, Cowling K, Bagnall NH, Hines BM, Ruffell AP, Hunt PW, et al. Relative level of thiabendazole resistance associated with the E198A and F200Y SNPs in larvae of a multi-drug resistant isolate of Haemonchus contortus. Int J Parasitol Drugs Drug Resist. 2012;2:92–7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  295. Chaudhry U, Miller M, Yazwinski T, Kaplan R, Gilleard J. The presence of benzimidazole resistance mutations in Haemonchus placei from US cattle. Vet Parasitol. 2014;204(3–4):411–5.

    Article  CAS  PubMed  Google Scholar 

  296. Encalada-Mena L, Tuyub-Solis H, Ramirez-Vargas G, Mendoza-de-Gives P, Aguilar-Marcelino L, Lopez-Arellano ME. Phenotypic and genotypic characterisation of Haemonchus spp. and other gastrointestinal nematodes resistant to benzimidazole in infected calves from the tropical regions of Campeche State, Mexico. Vet Parasitol. 2014;205(1–2):246–54.

    Article  CAS  PubMed  Google Scholar 

  297. Elard L, Cabaret J, Humbert JF. PCR diagnosis of benzimidazole-susceptibility or resistance in natural populations of the small ruminant parasite, Teladorsagia circumcincta. Vet Parasitol. 1999;80(3):231–7.

    Article  CAS  PubMed  Google Scholar 

  298. Silvestre A, Humbert JF. Diversity of benzimidazole-resistance alleles in populations of small ruminant parasites. Int J Parasitol. 2002;32(7):921–8.

    Article  CAS  PubMed  Google Scholar 

  299. Tiwari J, Kumar S, Kolte AP, Swarnkar CP, Singh D, Pathak KM. Detection of benzimidazole resistance in Haemonchus contortus using RFLP-PCR technique. Vet Parasitol. 2006;138(3–4):301–7.

    Article  CAS  PubMed  Google Scholar 

  300. Williamson SM, Storey B, Howell S, Harper KM, Kaplan RM, Wolstenholme AJ. Candidate anthelmintic resistance-associated gene expression and sequence polymorphisms in a triple-resistant field isolate of Haemonchus contortus. Mol Biochem Parasitol. 2011;180(2):99–105.

    Article  CAS  PubMed  Google Scholar 

  301. Knapp-Lawitzke F, Krucken J, Ramunke S, von Samson-Himmelstjerna G, Demeler J. Rapid selection for beta-tubulin alleles in codon 200 conferring benzimidazole resistance in an Ostertagia ostertagi isolate on pasture. Vet Parasitol. 2015;209(1–2):84–92.

    Article  CAS  PubMed  Google Scholar 

  302. 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 (Cyathostomins) indicates that the TAC allele is only moderately selected in benzimidazole-resistant populations. Parasitology. 2003;127(5):489–96.

    Article  CAS  Google Scholar 

  303. 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(1):53–9.

    Article  CAS  PubMed  Google Scholar 

  304. Drogemuller M, Schnieder T, von Samson-Himmelstjerna G. Beta-tubulin complementary DNA sequence variations observed between cyathostomins from benzimidazole-susceptible and -resistant populations. J Parasitol. 2004;90(4):868–70.

    Article  CAS  PubMed  Google Scholar 

  305. Hodgkinson JE, Clark HJ, Kaplan RM, Lake SL, Matthews JB. The role of polymorphisms at beta tubulin isotype 1 codons 167 and 200 in benzimidazole resistance in cyathostomins. Int J Parasitol. 2008;38(10):1149–60.

    Article  CAS  PubMed  Google Scholar 

  306. Walsh TK, Donnan AA, Jackson F, Skuce P, Wolstenholme AJ. Detection and measurement of benzimidazole resistance alleles in Haemonchus contortus using real-time PCR with locked nucleic acid Taqman probes. Vet Parasitol. 2007;144(3–4):304–12.

    Article  CAS  PubMed  Google Scholar 

  307. Hoglund J, Gustafsson K, Ljungstrom BL, Engstrom A, Donnan A, Skuce P. Anthelmintic resistance in Swedish sheep flocks based on a comparison of the results from the faecal egg count reduction test and resistant allele frequencies of the beta-tubulin gene. Vet Parasitol. 2009;161(1-2):60–8.

    Article  PubMed  CAS  Google Scholar 

  308. Martinez-Valladares M, Donnan A, Geldhof P, Jackson F, Rojo-Vazquez FA, Skuce P. Pyrosequencing analysis of the beta-tubulin gene in Spanish Teladorsagia circumcincta field isolates. Vet Parasitol. 2012;184(2–4):371–6.

    Article  CAS  PubMed  Google Scholar 

  309. Barrere V, Falzon LC, Shakya KP, Menzies PI, Peregrine AS, Prichard RK. Assessment of benzimidazole resistance in Haemonchus contortus in sheep flocks in Ontario, Canada: comparison of detection methods for drug resistance. Vet Parasitol. 2013;198(1–2):159–65.

    Article  CAS  PubMed  Google Scholar 

  310. Mezo M, Gonzalez-Warleta M, Carro C, Ubeira FM. An ultrasensitive capture ELISA for detection of Fasciola hepatica coproantigens in sheep and cattle using a new monoclonal antibody (MM3). J Parasitol. 2004;90(4):845–52.

    Article  PubMed  Google Scholar 

  311. Gordon DK, Zadoks RN, Stevenson H, Sargison ND, Skuce PJ. On farm evaluation of the coproantigen ELISA and coproantigen reduction test in Scottish sheep naturally infected with Fasciola hepatica. Vet Parasitol. 2012;187(3–4):436–44.

    Article  CAS  PubMed  Google Scholar 

  312. Novobilský A, Averpil HB, Höglund J. The field evaluation of albendazole and triclabendazole efficacy against Fasciola hepatica by coproantigen ELISA in naturally infected sheep. Vet Parasitol. 2012;190(1–2):272–6.

    Article  PubMed  CAS  Google Scholar 

  313. Waghorn TS, Leathwick DM, Rhodes AP, Lawrence KE, Jackson R, Pomroy WE, et al. Prevalence of anthelmintic resistance on sheep farms in New Zealand. N Z Vet J. 2006;54(6):271–7.

    Article  CAS  PubMed  Google Scholar 

  314. Van Wyk JA, Stenson MO, Van der Merwe JS, Vorster RJ, Viljoen PG. Anthelmintic resistance in South Africa: surveys indicate an extremely serious situation in sheep and goat farming. Onderstepoort Vet J. 1999;66(4):273–84.

    Google Scholar 

  315. Veríssimo CJ, Niciura SCM, Alberti ALL, Rodrigues CFC, Barbosa CMP, Chiebao DP, et al. Multidrug and multispecies resistance in sheep flocks from São Paulo state, Brazil. Vet Parasitol. 2012;187(1–2):209–16.

    Article  PubMed  Google Scholar 

  316. Love SC, Neilson FJ, Biddle AJ, McKinnon R. Moxidectin-resistant Haemonchus contortus in sheep in northern New South Wales. Aust Vet J. 2003;81(6):359–60.

    Article  CAS  PubMed  Google Scholar 

  317. Tsotetsi AM, Njiro S, Katsande TC, Moyo G, Baloyi F, Mpofu J. Prevalence of gastrointestinal helminths and anthelmintic resistance on small-scale farms in Gauteng Province, South Africa. Trop Anim Health Prod. 2013;45(3):751–61.

    Article  PubMed  Google Scholar 

  318. Howell SB, Burke JM, Miller JE, Terrill TH, Valencia E, Williams MJ, et al. Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. J Am Ved Med Assoc. 2008;233(12):1913–9.

    Article  Google Scholar 

  319. Mederos AE, Banchero GE, Ramos Z. First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay. Parasit Vectors. 2014;7(1):598–601.

    Article  PubMed  PubMed Central  Google Scholar 

  320. Vatta A, Lindberg A. Managing anthelmintic resistance in small ruminant livestock of resource-poor farmers in South Africa: review article. J S Afr Vet Assoc. 2006;77(1):2–8.

    Article  Google Scholar 

  321. Rose H, Rinaldi L, Bosco A, Mavrot F, de Waal T, Skuce P, et al. Widespread anthelmintic resistance in European farmed ruminants: a systematic review. Vet Rec. 2015;176(21):546.

    Article  CAS  PubMed  Google Scholar 

  322. Martínez-Valladares M, Martínez-Pérez JM, Robles-Pérez D, Cordero-Perez C, Famularo M, Fernandez-Pato N, et al. The present status of anthelmintic resistance in gastrointestinal nematode infections of sheep in the northwest of Spain by in vivo and in vitro techniques. Vet Parasitol. 2013;191(1):177–81.

    Article  PubMed  CAS  Google Scholar 

  323. Peña-Espinoza M, Thamsborg SM, Demeler J, Enemark HL. Field efficacy of four anthelmintics and confirmation of drug-resistant nematodes by controlled efficacy test and pyrosequencing on a sheep and goat farm in Denmark. Vet Parasitol. 2014;206(3–4):208–15.

    Article  PubMed  CAS  Google Scholar 

  324. Chandrawathani P, Waller PJ, Adnan M, Hoglund J. Evolution of high-level, multiple anthelmintic resistance on a sheep farm in Malaysia. Trop Anim Health Prod. 2003;35(1):17–25.

    Article  CAS  PubMed  Google Scholar 

  325. Le Jambre LF, Geoghegan J, Lyndal-Murphy M. Characterization of moxidectin resistant Trichostrongylus colubriformis and Haemonchus contortus. Vet Parasitol. 2005;128(1–2):83–90.

    Article  PubMed  CAS  Google Scholar 

  326. Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter? Vet Parasitol. 2014;201(1):1–8.

    Article  CAS  PubMed  Google Scholar 

  327. Alvarez-Sanchez MA, Mainar-Jaime RC, Perez-Garcia J, Rojo-Vazquez FA. Resistance of Fasciola hepatica to triclabendazole and albendazole in sheep in Spain. Vet Rec. 2006;159(13):424–5.

    Article  CAS  PubMed  Google Scholar 

  328. Coles GC, Stafford KA. Activity of oxyclozanide, nitroxynil, clorsulon and albendazole against adult triclabendazole-resistant Fasciola hepatica. Vet Rec. 2001;148(23):723–4.

    Article  CAS  PubMed  Google Scholar 

  329. Brennan GP, Fairweather I, Trudgett A, Hoey E, McCoy M, McConville M, et al. Understanding triclabendazole resistance. Exp Mol Pathol. 2007;82(2):104–9.

    Article  CAS  PubMed  Google Scholar 

  330. Waghorn TS, Leathwick DM, Rhodes AP, Lawrence KE, Jackson R, Pomroy WE, et al. Prevalence of anthelmintic resistance on 62 beef cattle farms in the North Island of New Zealand. N Z Vet J. 2006;54(6):278–82.

    Article  CAS  PubMed  Google Scholar 

  331. Cotter JL, Van Burgel A, Besier RB. Anthelmintic resistance in nematodes of beef cattle in south-west Western Australia. Vet Parasitol. 2015;207(3–4):276–84.

    Article  CAS  PubMed  Google Scholar 

  332. Becerra-Nava R, Alonso-Díaz M, Fernández-Salas A, Quiroz R. First report of cattle farms with gastrointestinal nematodes resistant to levamisole in Mexico. Vet Parasitol. 2014;204(3–4):285–90.

    Article  CAS  PubMed  Google Scholar 

  333. Rendell DK. Anthelmintic resistance in cattle nematodes on 13 south-west Victorian properties. Aust Vet J. 2010;88(12):504–9.

    Article  CAS  PubMed  Google Scholar 

  334. Anziani OS, Zimmermann G, Guglielmone AA, Vazquez R, Suarez V. Avermectin resistance in Cooperia pectinata in cattle in Argentina. Vet Rec. 2001;149(2):58–9.

    Article  CAS  PubMed  Google Scholar 

  335. Bartley DJ, McArthur CL, Devin LM, Sutra JF, Morrison AA, Lespine A, et al. Characterisation of macrocyclic lactone resistance in two field-derived isolates of Cooperia oncophora. Vet Parasitol. 2012;190(3–4):454–60.

    Article  CAS  PubMed  Google Scholar 

  336. Mejia ME, Fernandez Igartua BM, Schmidt EE, Cabaret J. Multispecies and multiple anthelmintic resistance on cattle nematodes in a farm in Argentina: the beginning of high resistance? Vet Res. 2003;34(4):461–7.

    Article  CAS  PubMed  Google Scholar 

  337. Soutello RGV, Seno MCZ, Amarante AFT. Anthelmintic resistance in cattle nematodes in northwestern São Paulo State, Brazil. Vet Parasitol. 2007;148(3–4):360–4.

    Article  CAS  PubMed  Google Scholar 

  338. Moll L, Gaasenbeek CPH, Vellema P, Borgsteede FHM. Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in The Netherlands. Vet Parasitol. 2000;91(1–2):153–8.

    Article  CAS  PubMed  Google Scholar 

  339. Reinemeyer CR. Anthelmintic resistance in non-strongylid parasites of horses. Vet Parasitol. 2012;185(1):9–15.

    Article  CAS  PubMed  Google Scholar 

  340. Stratford CH, Lester HE, Pickles KJ, McGorum BC, Matthews JB. An investigation of anthelmintic efficacy against strongyles on equine yards in Scotland. Equine Vet J. 2014;46(1):17–24.

    Article  CAS  PubMed  Google Scholar 

  341. Armstrong SK, Woodgate RG, Gough S, Heller J, Sangster NC, Hughes KJ. The efficacy of ivermectin, pyrantel and fenbendazole against Parascaris equorum infection in foals on farms in Australia. Vet Parasitol. 2014;205(3–4):575–80.

    Article  CAS  PubMed  Google Scholar 

  342. Slocombe JOD, de Gannes RV, Lake MC. Macrocyclic lactone-resistant Parascaris equorum on stud farms in Canada and effectiveness of fenbendazole and pyrantel pamoate. Vet Parasitol. 2007;145(3):371–6.

    Article  CAS  PubMed  Google Scholar 

  343. Wolf D, Hermosilla C, Taubert A. Oxyuris equi: lack of efficacy in treatment with macrocyclic lactones. Vet Parasitol. 2014;201(1–2):163–8.

    Article  CAS  PubMed  Google Scholar 

  344. Coles GC, Brown SN, Trembath CM. Pyrantel-resistant large strongyles in racehorses. Vet Rec. 1999;145(14):408–10.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Animal and Veterinary Sciences, Charles Sturt University, Wagga Wagga, 2678, NSW, Australia

    R. G. Woodgate BSc, BVMS(Hons), PhD, GCLTHE & N. C. Sangster B.Sc.(Vrt.), B.F.Sc., Ph.D.

  2. School of Animal and Veterinary Sciences and Graham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, NSW, Australia

    A. J. Cornell

Authors
  1. R. G. Woodgate BSc, BVMS(Hons), PhD, GCLTHE
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. J. Cornell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. C. Sangster B.Sc.(Vrt.), B.F.Sc., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. G. Woodgate BSc, BVMS(Hons), PhD, GCLTHE .

Editor information

Editors and Affiliations

  1. Treiber Therapeutics, Cambridge, Massachusetts, USA

    Douglas L. Mayers

  2. Wayne State University School of Medicine, Detroit Medical Center, Detroit, Michigan, USA

    Jack D. Sobel

  3. Canada Research Chair in Antimicrobial Resistance, Centre de recherche en Infectiologie, University of Laval, Quebec City, Canada

    Marc Ouellette

  4. Division of Infectious Diseases, University of Michigan Medical School, Ann Arbor, Michigan, USA

    Keith S. Kaye

  5. Infection Control and Prevention Unit of Infectious Diseases, Assaf Harofeh Medical Center, Sackler Faculty of Medicine, Tel-Aviv University, Tel Aviv, Israel

    Dror Marchaim

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Woodgate, R.G., Cornell, A.J., Sangster, N.C. (2017). Occurrence, Measurement and Clinical Perspectives of Drug Resistance in Important Parasitic Helminths of Livestock. In: Mayers, D., Sobel, J., Ouellette, M., Kaye, K., Marchaim, D. (eds) Antimicrobial Drug Resistance. Springer, Cham. https://doi.org/10.1007/978-3-319-47266-9_30

Download citation

Publish with us

Policies and ethics

Search

Navigation