Skip to main content
SpringerLink
Log in

Therapeutic efficacy of triclabendazole in comparison to combination of triclabendazole and levamisole in sheep naturally infected with Fasciola sp.

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

Fascioliasis is an important parasitic disease which affects productivity of ruminants, and imposes significant economic losses. Benzimidazoles are effective in the treatment of fascioliasis; however, there are several reports on benzimidazoles resistant flukes. Combinational therapy is an approach to delay the emergence of resistant flukes. The present study aimed to compare the efficacy of triclabendazole (TBZ) and combination of triclabendazole and levamisole (TBZ + LVM) in the treatment of sheep naturally infected with Fasciola sp. For this purpose, 40 ewes infected with Fasciola sp. in three groups received TBZ, and TBZ + LVM, or remained untreated as CON. Fecal egg count (FEC), fecal egg count reduction (FECR), liver enzymes activity, albumin, globulin, and total protein levels were measured on day 0, 7, 14, and 28 post treatments. Obtained results showed that treatment with TBZ and TBZ + LVM resulted in significant reduction in FEC (P < 0.05), and FECR reached to values of higher than 90% on 28 day post treatment. The FEC for TBZ + LMV on day 7 and 14 were 12.25 ± 3.82 and 3.08 ± 1.03, respectively which was significantly lower in comparison to TBZ and CON (P < 0.05). Efficacy of TBZ + LMV was higher than TBZ on day 7 and 14 post treatment; however, no significant difference was observed on 28 day. The liver enzyme activities on days 7 and 14 were lower in the TBZ + LVM sheep in comparison to the TBZ and CON. Treatment with TBZ or TBZ + LVM resulted in an increase in albumin and a decrease in globulin. Over all, the present study clarified the importance of combinational therapy, and demonstrated that combination of TBZ + LVM resulted in higher efficacy and earlier improvement of liver conditions in sheep naturally infected with Fasciola sp.

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

  • Anderson N, Martin PJ, Jarrett RG (1988) Mixtures of anthelmintics: a strategy against resistance. Aust Vet J 65(2):62–64

    Article  CAS  Google Scholar 

  • Cabaret J, Berrag B (2004) Faecal egg count reduction test for assessing anthelmintic efficacy: average versus individually based estimations. Vet Parasitol 121(1–2):105–113

    Article  CAS  Google Scholar 

  • Ciuffa AZ, Urzedo MCC, Silva DM, Pires BC, Rezende LM, Brasão SC, Macedo Júnior GDL, Rosalinski-Moraes F (2017) Effectiveness of monepantel and levamisole to control gastrointestinal strongylid parasites of sheep. Biosci J. https://doi.org/10.14393/BJ-v33n3-33325

    Article  Google Scholar 

  • Coles GC, Bauer C, Borgsteede FHM, 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(1–2):35–44

    Article  CAS  Google Scholar 

  • Conceição MAP, Durão RM, Costa IH, da Costa JMC (2002) Evaluation of a simple sedimentation method (modified McMaster) for diagnosis of bovine fascioliosis. Vet Parasitol 105(4):337–343

    Article  Google Scholar 

  • de Waard J, Willem D, Wobbes T, de Man BM, van der Linden CJ, Hendriks T (1995) Post-operative levamisole may compromise early healing of experimental intestinal anastomoses. Br J Cancer 72(2):456–460

    Article  Google Scholar 

  • Eslami A, Hosseini SH, Meshgi B (2009) Animal fasciolosis in north of Iran. Iran J Publ Health 38(4):132–135

    Google Scholar 

  • Fairweather I, Brennan GP, Hanna REB, Robinson MW, Skuce PJ (2020) Drug resistance in liver flukes. Int J Parasitol Drugs Drug Resist 12:39–59

    Article  CAS  Google Scholar 

  • Findlay VL, Zilberg D, Munday BL (2000) Evaluation of levamisole as a treatment for amoebic gill disease of Atlantic salmon, Salmo salar L. J Fish Dis 23(3):193–198

    Article  CAS  Google Scholar 

  • Goraish IA, Abdelsalam EB, Tartour G, Abbas B, Aradaib IE (1988) The effect of levamisole (L. tetramisole) treatment on the susceptibility to Fasciola gigantica infection in goats. Revue D’élevage Et De Médecine Vétérinaire Des Pays Tropicaux 41(3):283–287

    CAS  PubMed  Google Scholar 

  • Ibrahim N (2017) Fascioliasis: systematic review. Adv Biol Res 11(5):278–285

    Google Scholar 

  • Kelley JM, Elliott TP, Beddoe T, Anderson G, Skuce P, Spithill TW (2016) Current threat of triclabendazole resistance in Fasciola hepatica. Trends Parasitol 32(6):458–469

    Article  CAS  Google Scholar 

  • Khosravi A, Babaahmady E (2012) Epidemiology of Fasciola hepatica in Iran. Int J Biol 4(4):86–90

    Article  Google Scholar 

  • Kozat S, Denizhan V (2010) Glucose, lipid, and lipoprotein levels in sheep naturally infected with Fasciola hepatica. J Parasitol 96(3):657–659

    Article  Google Scholar 

  • Martínez-Valladares M, del Rosario Famularo M, Fernández-Pato N, Castañón-Ordóñez L, Cordero-Pérez C, Rojo-Vázquez FA (2010) Efficacy of nitroxynil against Fasciola hepatica resistant to triclabendazole in a naturally infected sheep flock. Parasitol Res 107(5):1205–1211

    Article  Google Scholar 

  • Martínez-Valladares M, Robles-Pérez D, Martínez-Pérez JM, Cordero-Pérez C, del Rosario Famularo M, Fernández-Pato N, González-Lanza C, Castañón-Ordóñez L, Rojo-Vázquez FA (2013) Prevalence of gastrointestinal nematodes and Fasciola hepatica in sheep in the northwest of Spain: relation to climatic conditions and/or man-made environmental modifications. Parasites Vectors 6(1):1–9

    Article  Google Scholar 

  • Martínez-Valladares M, Cordero-Pérez C, Rojo-Vázquez FA (2014) Efficacy of an anthelmintic combination in sheep infected with Fasciola hepatica resistant to albendazole and clorsulon. Exp Parasitol 136:59–62

    Article  Google Scholar 

  • Matanović K, Severin K, Martinković F, Šimpraga M, Janicki Z, Barišić J (2007) Hematological and biochemical changes in organically farmed sheep naturally infected with Fasciola hepatica. Parasitol Res 101(6):1657–1661

    Article  Google Scholar 

  • Mavromati J, Hamzaraj E, Zanaj S, Mavromati E, Raikos N, Giadinis ND, Shabani E (2016) The monitoring of some anthelmintic results in control of fasciolosis in extensive system dairy sheep in Albania. ANGLISTICUM. J Assoc-Inst Engl Lang Am Stud 2(4):205–213

    Google Scholar 

  • Mitchell GBB, Armour J (1981) Stimulation of resistance to Fasciola hepatica infection in sheep by a regime involving the use of the immunomodulatory compound L tetramisole (levamisole). Res Vet Sci 30(3):343–348

    Article  CAS  Google Scholar 

  • Moghaddam AS, Massoud J, Mahmoodi M, Mahvi AH, Periago MV, Artigas P, Mas-Coma S (2004) Human and animal fascioliasis in Mazandaran province, northern Iran. Parasitol Res 94(1):61–69

    Article  CAS  Google Scholar 

  • Moll L, Gaasenbeek CPH, Vellema P, Borgsteede FHM (2000) Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in The Netherlands. Vet Parasitol 91(1–2):153–158

    Article  CAS  Google Scholar 

  • Novobilský A, Solis NA, Skarin M, Höglund J (2016) Assessment of flukicide efficacy against Fasciola hepatica in sheep in Sweden in the absence of a standardised test. Int J Parasitol Drugs Drug Resist 6(3):141–147

    Article  Google Scholar 

  • Pal S, Dasgupta CK (2006) Haemato-biochemical profiles of buffalo in anthelmintics treatment against Fasciola gigantica infection. Buffalo Bull 25(2):40

    Google Scholar 

  • Pérez-Caballero R, Siles-Lucas M, González-Miguel J, Martínez-Moreno FJ, Escamilla A, Pérez J, Buffoni L (2018) Pathological, immunological and parasitological study of sheep vaccinated with the recombinant protein 14-3-3z and experimentally infected with Fasciola hepatica. Vet Immunol Immunopathol 202:115–121

    Article  Google Scholar 

  • Sajid MS, Iqbal Z, Muhammad G, Iqbal MU (2006) Immunomodulatory effect of various anti-parasitics: a review. Parasitology 132(3):301

    Article  CAS  Google Scholar 

  • Scott PR, Sargison ND, Macrae A, Rhind SR (2005) An outbreak of subacute fasciolosis in Soay sheep: ultrasonographic biochemical and histological studies. Vet J 170(3):325–331

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to express their gratitude to Dr. Sooud Rouhani, veterinarian practitioner for his help and supports during the study. This study was partly supported by Amol University of Special Modern Technologies, Amol, Iran.

Author information

Authors and Affiliations

  1. Faculty of Veterinary Medicine, Amol University of Special Modern Technologies, Amol, Iran

    Mohaddeseh Abouhosseini Tabari, Shohre Alian Samakkhah & Atefeh Araghi

  2. Faculty of Veterinary Medicine, Islamic Azad University, Babol-Branch, Babol, Iran

    Seyed Aria Fallah Vahdati

  3. Department of Veterinary Parasitology, Islamic Azad University, Babol-Branch, Babol, Iran

    Mohammad Reza Youssefi

  4. Department of Medical Sciences, Comprehensive Health Research Center, Islamic Azad University, Babol Branch, Babol, Iran

    Mohammad Reza Youssefi

Authors
  1. Mohaddeseh Abouhosseini Tabari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Seyed Aria Fallah Vahdati
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shohre Alian Samakkhah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Atefeh Araghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammad Reza Youssefi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohammad Reza Youssefi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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

Tabari, M.A., Vahdati, S.A.F., Samakkhah, S.A. et al. Therapeutic efficacy of triclabendazole in comparison to combination of triclabendazole and levamisole in sheep naturally infected with Fasciola sp.. J Parasit Dis 46, 80–86 (2022). https://doi.org/10.1007/s12639-021-01422-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-021-01422-w

Keywords

Search

Navigation