Skip to main content
SpringerLink
Log in

Field and Molecular Evaluation of Anthelmintic Resistance of Nematode Populations from Cattle and Sheep Naturally Infected Pastured on Mixed Grazing areas at Rio Grande do Sul, Brazil

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Background

Reports of a lack of efficacy of most of the anthelmintic compounds for ruminants associated with the long-time necessity for creating new molecules have stressed the urgency to adopt alternative methods to control gastrointestinal parasites infection, such as strategies of sharing grazing areas. Therefore, this study aimed to evaluate nematode populations affecting cattle and sheep that share grazing areas before and after treatment with different anthelmintic compounds, and investigate the efficacy of anthelmintic treatment in these naturally infected ruminants at farms in the state of Rio Grande do Sul, Brazil.

Methods

The presence of co-infections by Haemonchus species was investigated by polymerase chain reaction (PCR) for groups treated with a benzimidazole. Farms were selected by: farmers’ consent, presence of 42–60 (or more) calves and sheep per farm with counts of ≥ 200 eggs per gram of feces (EPG), availability of calves and lambs aging from 6 to 9 months, absence of anthelmintic treatment for both species for 60 days before the experimental period, and shared grazing areas between this species on each farm. Animals were distributed into six treatment groups for each ruminant species per farm and treated with: ivermectin, doramectin, moxidectin, levamisole, albendazole, and closantel.

Results

Levamisol was the most effective anthelmintic compound for both ruminant species. In general, Cooperia spp., Haemonchus spp., and Trichostrongylus spp. were the genus present after tested treatments that were ineffective. PCR showed the presence of Haemonchus species co-infections between cattle and sheep.

Conclusion

Therefore, this study demonstrated the similarity between nematode population, the presence of multi-resistant nematodes, and the presence of Haemonchus species co-infections affecting different ruminant species that share pastures.

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

Similar content being viewed by others

References

  1. Achi YL, Zinsstag J, Yao K, Yeo N, Dorchies P, Jacquiet P (2003) Host specificity of Haemonchus spp. for domestic ruminants in the savanna in northern Ivory Coast. Vet Parasitol 116:151–158

    Article  CAS  Google Scholar 

  2. Amarante AFT, Amarante MRV (2016) Advances in the diagnosis of the gastrointestinal nematode infections in ruminants. Braz J Vet Res Anim Sci 53:127–137

    Article  Google Scholar 

  3. Amarante MRV, Santos MC, Bassetto CC, Amarante AFT (2017) PCR primers for straightforward differentiation of Haemonchus contortus, Haemonchus placei and their hybrids. J Helminthol 91(6):757–776

    Article  CAS  Google Scholar 

  4. Amarante AF, Bagnola Junior J, Amarante MR, Barbosa MA (1997) Host specificity of sheep and cattle nematodes in Sao Paulo state, Brazil. Vet Parasitol 73:89–104

    Article  CAS  Google Scholar 

  5. Bekelaar K, Waghorn T, Tavendale M, McKenzie C, Leathwick D (2018) Heat shock, but not temperature, is a biological trigger for the exsheathment of third-stage larvae of Haemonchus contortus. Parasitol Res 117:2395–2402

    Article  Google Scholar 

  6. Brasil BS, Nunes RL, Bastianetto E, Drummond MG, Carvalho DC, Leite RC, Molento MB, Oliveira DA (2012) Genetic diversity patterns of Haemonchus placei and Haemonchus contortus populations isolated from domestic ruminants in Brazil. Int J Parasitol 42:469–479

    Article  Google Scholar 

  7. Burgess CGS, Bartley Y, Redman E, Skuce PJ, Nath M, Whitelaw F, Tait A, Gilleard JS, Jackson F (2012) A survey of the trichostrongylid nematode species present on UK sheep farms and associated anthelmintic control practices. Vet Parasitol 189:299–307

    Article  CAS  Google Scholar 

  8. Cezar AS, Catto JB, Bianchin I (2008) Alternative control of the gastrointestinal nematodes of the ruminants: actuality and perspectives. Cienc Rural 8:2083–2091

    Article  Google Scholar 

  9. Cezar AS, Toscan G, Camillo G, Sangioni LA, Ribas HO, Vogel FSF (2010) Multiple resistance of gastrointestinal nematodes to nine different skid drugs in the sheep flock in southern Brazil. Vet Parasitol 173:157–160

    Article  Google Scholar 

  10. Charlier J, Morgan ER, Rinaldi L, van Dijk J, Demeler J, Höglund J, Hertzberg H, Van Ranst B, Hendrickx G, Vercruysse J, Kenyon F (2014) Practices to optimise gastrointestinal nematode control on sheep, goat and cattle farms in Europe using targeted (selective) treatments. Vet Rec 175(10):250–255

    Article  CAS  Google Scholar 

  11. Chaudhry U, Elizabeth M, Redman EM, Abbas M, Muthusamy R, Ashraf K, Gilleard JS (2015) Genetic evidence for hybridisation between Haemonchus contortus and Haemonchus placei in natural field populations and its implications for interspecies transmission of anthelmintic resistance. Int J Parasitol 45:149–159

    Article  CAS  Google Scholar 

  12. Coles GC, Bauer C, Borgsteede FH, Geerts S, Klei TR, Taylor MA, Waller PJ (1992) World Association for the Advancement of Veterinary Parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 44:35–44

    Article  CAS  Google Scholar 

  13. Coles GC, Jackson F, Pomroy WE, Prichard RK, Samson-Himmelstjerna GV, Silvestre A, Taylor MA, Vercruysse J (2006) The detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol 136:167–185

    Article  CAS  Google Scholar 

  14. Cristel S, Fiel C, Anziani O, Descarga C, Cetrá B, Romero J, Fernández S, Entrocasso C, Lloberasi M, Medus D, Steffan P (2017) Anthelmintic resistance in grazing beef cattle in central and northeastern areas of Argentina—an update. Vet Parasitol Reg Stud Rep 9:25–28

    Google Scholar 

  15. Fernandes LH, Seno MCZ, Amarante AFT, Souza H, Belluzzo CEC (2004) Efeito do pastejo rotacionado e alternado com bovinos adultos no controle da verminose em ovelhas. Arq Bras Med Vet Zootec 56:733–740

    Article  Google Scholar 

  16. Gasbarre LC, Smith LL, Hoberg E, Pilitt PA (2009) Further characterization of a cattle nematode population with demonstrated resistance to current anthelmintics. Vet Parasitol 166:275–280

    Article  CAS  Google Scholar 

  17. Gasbarre LC, Smith LL, Lichtenfels JR, Pilitt PA (2009) The identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle population in the US. Vet Parasitol 166:281–285

    Article  CAS  Google Scholar 

  18. Hussain T, Periasamy K, Nadeem A, Babar ME, Pichler R, Diallo A (2014) Sympatric species distribution, genetic diversity and population structure of Haemonchus isolates from domestic ruminants in Pakistan. Vet Parasitol 206:188–199

    Article  Google Scholar 

  19. Jacquiet P, Cabaret J, Thiam E, Cheikh D (1998) Experimental and natural Haemonchus spp. cross infections of domestic ruminants in Sahelian West Africa. Ann NY Acad Sci 849:465–469

    Article  CAS  Google Scholar 

  20. Lichtenfels JR, Pilitt PA, Hoberg EP (1994) New morphological characters for identifying individual specimens of Haemonchus spp. (Nematoda: Trichostrongyloidea) and a key to species in ruminants of North America. J Parasitol 80:107–111

    Article  CAS  Google Scholar 

  21. Lopes WDZ, Felippelli G, Teixeira WFP, Cruz BC, Maciel WG, Buzzulini C, Matos LVS, Gomes LVC, Pereira JCM, Fávero FC, Oliveira GP, Costa AJ (2014) Haemonchus placei, Cooperia punctata and Oesophagostomum radiatum resistant to ivermectin pour-on 500 mcg kg-1 in cattle from Brazil. Cienc Rural 44:847–853

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Marley CL, Fraser MD, Davies DA, Rees ME, Vale JE, Forbes AB (2006) The effect of mixed or sequential grazing of cattle and sheep on the faecal egg counts and growth rates of weaned lambs when treated with anthelmintics. Vet Parasitol 142:134–141

    Article  CAS  Google Scholar 

  24. Minho AP, Gaspar EB, Yoshihara E (2015) Manual de Técnicas Laboratoriais e de Campo para a Realização de Ensaios Experimentais em Parasitologia Veterinária: Foco em Helmintos Gastrintestinais de Ruminantes 148:1–33. https://ainfo.cnptia.embrapa.br/digital/bitstream/item/136882/1/DT-148-online.pdf. Accessed 3 May 2017

  25. Molento MB, Verissimo CJ, Amarante AT, Van Wyk JA, Chagas ACS, Araújo JV, Borges FA (2013) Alternatives for the control of gastrointestinal nematoides of small ruminants. Arq Inst Biol São Paulo 80:253–263

    Article  Google Scholar 

  26. Neves JHD, Carvalho N, Rinaldi L, Cringoli G, Amarante AFT (2014) Diagnosis of anthelmintic resistance in cattle in Brazil: a comparison of different methodologies. Vet Parasitol 206:216e226

    Article  Google Scholar 

  27. Pinheiro AC (1983) Verminose ovina. Hora Vet 12:5–9

    Google Scholar 

  28. Pinheiro AC, Echevarria FAM, Branco FPJA, Macedo JBRR (1987). Descontaminação da pastagem de ovinos pelo pastoreio alternado com bovinos. In: Coletânea das Pesquisas: Medicina Veterinária—Parasitologia. EMBRAPA, Centro Nacional de Pesquisa de Ovinos, 275–278

  29. Ramos F, Portella PL, Rodrigues deSF, Reginato ZC, Pötter L, Cezar SA, Sangioni LA, Vogel FSF (2016) Anthelmintic resistance in gastrointestinal nematodes of beef cattle in the state of Rio Grande do Sul, Brazil. IJP Drugs Drug Resist 6(1):93–101

    Article  Google Scholar 

  30. Rocha RA, Bresciani KDS, Barros TFM, Fernandes LH, Silva MB, Amarante AFT (2008) Sheep and cattle grazing alternately: nematode parasitism and pasture decontamination. Small Rumin Res 75(2–3):135–143

    Article  Google Scholar 

  31. Santiago MAM, Costa UC, Benevenga SF (1975) Estudo comparativo da prevalência de helmintos em ovinos e bovinos criados na mesma pastagem. Pesq Agropecu Bras 10:51–56

    Google Scholar 

  32. Santos VRV (2010) Efeito dos sistemas de pastejo isolado, simultâneo e alternado de ovinos com bovinos sobre as características da forragem, desempenho, consumo e características de carcaça dos ovinos, (unpublished PhD thesis, University of Brasília)

  33. Sargison ND, Jackson F, Bartley DJ, Wilson DJ, Stenhouse LJ, Penny CD (2007) Observations on the emergence of multiple anthelmintic resistance in sheep flocks in the southeast of Scotland. Vet Parasitol 145:65–76

    Article  CAS  Google Scholar 

  34. Sczesny-Moraes EA, Bianchin I, Silva KF, Catto JB, Honer MR, Paiva F (2010) Resistência anti-helmíntica de nematóides gastrintestinais em ovinos, Mato Grosso do Sul. Pesq Vet Bras 30:229–236

    Article  Google Scholar 

  35. Stephanie E, Gina LP, David JB, Jane EH, Jacqueline BM (2018) A survey of experiences of UK cattle and sheep farmers with anthelmintic prescribers; are best practice principles being deployed at farm level? Prev Vet Med 155:27–37

    Article  Google Scholar 

  36. Sutherland IA, Leathwick DM (2011) Anthelmintic resistance in nematode parasites of cattle: a global issue? Trends Parasitol 27:176–181

    Article  Google Scholar 

  37. Testi AJP (2015) AVALIAÇÃO DE TÉCNICAS DE CRIOPRESERVAÇÃO PARA MANUTENÇÃO DE LINHAGEM DE Haemonchus contortus EM LABORATÓRIO. Dissertation, State University of São Paulo (UNESP)

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

    Article  Google Scholar 

  39. Van Wyk JA, Mayhew E (2013) Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. J Vet Res 80:1–14

    Google Scholar 

Download references

Acknowledgements

The authors are grateful for the availability and collaboration of producers and their employees to carry out this work.

Author information

Authors and Affiliations

  1. Departamento de Medicina Veterinária Preventiva (DMVP), Centro de Ciências Rurais (CCR), Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, 97105-900, Brazil

    Fernanda Ramos, Camila Balconi Marques, Caroline Zamperete Reginato, Patricia Bräunig, Vanessa Osmari, Fagner Fernandes, Luis Antônio Sangioni & Fernanda Silveira Flôres Vogel

Authors
  1. Fernanda Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camila Balconi Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Caroline Zamperete Reginato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patricia Bräunig
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vanessa Osmari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fagner Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luis Antônio Sangioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fernanda Silveira Flôres Vogel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernanda Ramos.

Ethics declarations

Conflict of Interest

The authors of this manuscript have no financial or personal relationships with other people or organizations that could inappropriately influence or bias the content of the paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramos, F., Marques, C.B., Reginato, C.Z. et al. Field and Molecular Evaluation of Anthelmintic Resistance of Nematode Populations from Cattle and Sheep Naturally Infected Pastured on Mixed Grazing areas at Rio Grande do Sul, Brazil. Acta Parasit. 65, 118–127 (2020). https://doi.org/10.2478/s11686-019-00137-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-019-00137-6

Keywords

Search

Navigation