Skip to main content
SpringerLink
Log in

Characterization of a multidrug resistant Teladorsagia circumcincta isolate from Spain

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The aim of this work was to know the anthelmintic resistance (AR) status of a Spanish sheep flock infected by gastrointestinal nematodes (GIN) and the possible cross resistance among anthelmintics of the macrocyclic lactones (ML) family. The Faecal Egg Count Reduction Test (FECRT) was carried out to check the efficacy of albendazole (Zodalben®), levamisole (LEV) (Endex®) and an oral formulation of ivermectin (IVM) (Oramec®), at the recommended dose rates. Then, the study was extended to check the cross resistance between drugs of the ML family: injectable IVM (Ivomec®), oral moxidectin (Cydectin®), injectable moxidectin (Biodectin®) and doramectin (Dectomax®), at the recommended dose rates. The GIN species were identified after faecal cultures in all groups. The FECRT showed the resistance of a Teladorsagia circumcincta isolate against LEV (39–58%), IVM (88–92%) and doramectin (85%). This study is the first report to confirm the side resistance between these MLs, which belong to the avermectin chemical group, in a Spanish sheep flock. The in vitro efficacy of LEV and IVM was measured by the Larval Feeding Inhibition Assay (LFIA) using the IC50 measurement (concentration needed to inhibit the ingestion of 50% L1). The values of the multidrug resistant isolate were 0.25 μg/ml for LEV and 3 ng/ml for IVM. Both results were higher than the values obtained with a susceptible isolate, which could be indicative of AR. However, further research examining the response of a greater range of susceptible and resistant nematodes isolates should be carried out to establish a discrimination threshold.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Álvarez-Sánchez MA, Pérez García J, Bartley D, Jackson F, Rojo-Vázquez FA (2005) The larval feeding inhibition assay for the diagnosis of nematode anthelmintic resistance. Exp Parasitol 110:56–61

    Article  PubMed  Google Scholar 

  • Álvarez-Sánchez MA, Pérez-García J, Cruz-Rojo MA, Rojo-Vázquez FA (2006) Anthelmintic resistance in trichostrongylid nematodes of sheep farms in Northwest Spain. Parasitol Res 99:78–83

    Article  PubMed  Google Scholar 

  • Alvinerie M, Escudero E, Sutra JF, Eeckhoutte C, Galtier P (1998) The pharmacokinetics of moxidectin after oral and subcutaneous administration to sheep. Vet Parasitol 29:113–118

    CAS  Google Scholar 

  • Ardelli BF, Stitt LE, Tompkins JB, Prichard RK (2009) A comparison of the effects of ivermectin and moxidectin on the nematode Caenorhabditis elegans. Vet Parasitol 165:96–108

    Article  PubMed  CAS  Google Scholar 

  • Borgsteede FH, Dercksen DD, Huijbers R (2007) Doramectin and albendazole resistance in sheep in The Netherlands. Vet Parasitol 144:180–183

    Article  PubMed  CAS  Google Scholar 

  • Coles GC, Bauer C, Borgsteede FH, Geerts S, Klei TR, Taylor MA, Waller PJ (1992) 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 44:35–44

    Article  PubMed  CAS  Google Scholar 

  • Craig TM, Hatfield TA, Pankavich JA, Wang GT (1992) Efficacy of moxidectin against an ivermectin-resistant isolate of Haemonchus contortus in sheep. Vet Parasitol 41:329–333

    Article  PubMed  CAS  Google Scholar 

  • da Cruz DG, da Rocha LO, Arruda SS, Palieraqui JG, Cordeiro RC, Santos E Jr, Molento MB, Santos CdeP (2010) Anthelmintic efficacy and management practices in sheep farms from the state of Rio de Janeiro, Brazil. Vet Parasitol 170:340–343

    Article  PubMed  Google Scholar 

  • Díez-Baños P, Pedreira J, Sánchez-Andrade R, Francisco I, Suárez JL, Díaz P, Panadero R, Arias M, Painceira A, Paz-Silva A, Morrondo P (2008) Field evaluation for anthelmintic-resistant ovine gastrointestinal nematodes by in vitro and in vivo assays. J Parasitol 94:925–928

    Article  PubMed  Google Scholar 

  • Holmes PH (1993) Interactions between parasites and animal nutrition: the veterinary consequences. Proc Nutr Soc 52:113–120

    Article  PubMed  CAS  Google Scholar 

  • Kaminsky R, Gauvry N, Schorderet Weber S, Skripsky T, Bouvier J, Wenger A, Schroeder F, Desaules Y, Hotz R, Goebel T, Hosking BC, Pautrat F, Wieland-Berghausen S, Ducray P (2008) Identification of the amino-acetonitrile derivative monepantel (AAD 1566) as a new anthelmintic drug development candidate. Parasitol Res 103:931–939

    Article  PubMed  CAS  Google Scholar 

  • Kaminsky R, Bapst B, Stein PA, Strehlau GA, Allan BA, Hosking BC, Rolfe PF, Sager H (2010) Differences in efficacy of monepantel, derquantel and abamectin against multi-resistant nematodes of sheep. Parasitol Res, Epub ahead of print

  • Katiki LM, Chagas AC, Bizzo HR, Ferreira JF, Amarante AF (2011) Anthelmintic activity of Cymbopogon martinii, Cymbopogon schoenanthus and Mentha piperita essential oils evaluated in four different in vitro tests. Vet Parasitol 183:103–108

    Article  PubMed  CAS  Google Scholar 

  • Kopp SR, Coleman GT, McCarthy JS, Kotze AC (2008) Application of in vitro anthelmintic sensitivity assays to canine parasitology: detecting resistance to pyrantel in Ancylostoma caninum. Vet Parasitol 15:284–293

    Article  Google Scholar 

  • Lespine A, Martin S, Dupuy J, Roulet A, Pineau T, Orlowski S, Alvinerie M (2007) Interaction of macrocyclic lactones with P-glycoprotein: structure–affinity relationship. Eur J Pharm Sci 30:84–94

    Article  PubMed  CAS  Google Scholar 

  • Little PR, Hodges A, Watson TG, Seed JA, Maeder SJ (2010) Field efficacy and safety of an oral formulation of the novel combination anthelmintic, derquantel–abamectin, in sheep in New Zealand. NZ Vet J 58:121–129

    Article  CAS  Google Scholar 

  • MAFF (Ministry of Agriculture, Fisheries and Food) (1986) Manual of veterinary parasitology laboratory techniques, 3rd edn. GB, London

    Google Scholar 

  • Martínez-Valladares M, Cordero-Pérez C, Castañón-Ordóñez L, Famularo MR, Fernández-Pato N, Rojo-Vázquez FA (2010) Efficacy of a moxidectin/triclabendazole oral formulation against mixed infections of Fasciola hepatica and gastrointestinal nematodes in sheep. Vet Parasitol 174:166–169

    Article  PubMed  Google Scholar 

  • Njue AI, Hayashi J, Kinne L, Feng XP, Prichard RK (2004) Mutations in the extracellular domains of glutamate-gated chloride channel alpha3 and beta subunits from ivermectin-resistant Cooperia oncophora affect agonist sensitivity. J Neurochemistry 89:1137–1147

    Article  CAS  Google Scholar 

  • Novobilský A, Mueller-Harvey I, Thamsborg SM (2011) Condensed tannins act against cattle nematodes. Vet Parasitol 182:213–220

    Article  PubMed  Google Scholar 

  • Prichard R (1994) Anthelmintic resistance. Vet Parasitol 54:259–268

    Article  PubMed  CAS  Google Scholar 

  • Prichard RK, Hall CA, Kelly JD, Martin ICA, Donald AD (1980) The problem of anthelmintic resistance in nematodes. Aust Vet J 56:239–250

    Article  PubMed  CAS  Google Scholar 

  • Roberts FHS, O’Sullivan PJ (1950) Methods for egg counts and larval cultures for strongyles infecting. Aust J Agric Res 1:99–102

    Article  Google Scholar 

  • Sargison ND, Jackson F, Wilson DJ, Bartley DJ, Penny CD, Gilleard JS (2010) Characterisation of milbemycin-, avermectin-, imidazothiazole- and benzimidazole-resistant Teladorsagia circumcincta from a sheep flock. Vet Rec 29:681–686

    Article  Google Scholar 

  • Sheriff JC, Kotze AC, Sangster NC, Martin RJ (2002) Effects of macrocyclic lactone anthelmintics on feeding and pharyngeal pumping in Trichostrongylus colubriformis in vitro. Parasitology 125:477–484

    Article  PubMed  CAS  Google Scholar 

  • Traversa D, Paoletti B, Otranto D, Miller J (2007) First report of multiple drug resistance in trichostrongyles affecting sheep under field conditions in Italy. Parasitol Res 101:1713–1716

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study has been funded by Fort Dodge Veterinaria, S.A. Madrid and by the national project INIA-MEC, RTA2006-00183-C03-02. The work of Martínez-Valladares M. has been supported by a postdoctoral Jae-Doc contract from Consejo Superior de Investigaciones Científicas (CSIC).

Author information

Authors and Affiliations

  1. Instituto de Ganadería de Montaña, CSIC-ULE, Finca Marzanas, 24346, Grulleros, León, Spain

    M. Martínez-Valladares, C. Cordero-Pérez & F. A. Rojo-Vázquez

  2. Facultad de Veterinaria de León, Campus de Vegazana, 24071, León, Spain

    M. R. Famularo, N. Fernández-Pato, L. Castañón-Ordóñez & F. A. Rojo-Vázquez

Authors
  1. M. Martínez-Valladares
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. R. Famularo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Fernández-Pato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Cordero-Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Castañón-Ordóñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. A. Rojo-Vázquez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. A. Rojo-Vázquez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martínez-Valladares, M., Famularo, M.R., Fernández-Pato, N. et al. Characterization of a multidrug resistant Teladorsagia circumcincta isolate from Spain. Parasitol Res 110, 2083–2087 (2012). https://doi.org/10.1007/s00436-011-2753-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-011-2753-1

Keywords

Search

Navigation