The maintenance of anthelmintic efficacy in sheep in a Mediterranean climate

doi:10.1016/j.vetpar.2014.02.006

Veterinary Parasitology

Volume 203, Issues 1–2, 16 June 2014, Pages 139-143

https://doi.org/10.1016/j.vetpar.2014.02.006 Get rights and content

Abstract

To determine how far management practices on small ruminant dairy flocks in southern Italy have influenced the development of anthelmintic resistance (AR), faecal egg count (FEC) reduction tests were run on 54 sheep farms using the FLOTAC technique with a sensitivity of 2 eggs per gram of faeces. Tests were run on groups of sheep (12–20 animals per group) using six anthelmintics administered orally: levamisole on 8 farms, ivermectin (half and full dose) on 8 farms, moxidectin on 3 farms, monepantel on 8 farms, netobimin on 22 farms (pooled samples) and albendazole on 5 farms (pooled samples). Different formulae and statistics were used to calculate FEC reductions and confidence intervals based on the presence of a control group and/or the use of pooled samples. A very high average efficacy was obtained with all anthelmintics tested as follows: levamisole 99.3% (range across farms 98–100%), ivermectin half dose 99.5% (98.0–100%), ivermectin full dose 99.9% (99.3–100%), moxidectin 100% (99.9–100%), monepantel 99.4% (97–100%), netobimin 99.1% (92–100%) and albendazole 100%. The results suggest that the development of AR in small ruminants could be limited in countries with a Mediterranean type of climate provided that refugia of the nematode populations are maintained, anthelmintic use is restricted and movement of animals is not permitted to spread resistance.

Introduction

Anthelmintic resistance has become an urgent global issue in the control of nematodes of sheep and goats in major small ruminant producing regions, e.g. South America, Australasia, South Africa and the UK, with multiple resistance found on many farms. This is particularly true where Haemonchus contortus is the dominant species in summer rainfall areas. There is relatively little information on what is happening in sheep flocks in countries with a Mediterranean type climate, i.e. hot dry summers and cooler moist winters, with the exception of Greece (Papadopoulos et al., 2001) where mixing of flocks on mountain pastures may slow the development of resistance, and Algeria where benzimidazole resistance was found on five out of 14 pilot farms and ivermectin resistance on one (Bentounsi et al., 2007). However, in south-western Australia which also has a Mediterranean type climate resistance has been developing very rapidly (Suter et al., 2005). The climate in central and southern Italy is typically Mediterranean and in central Italy resistance to imidazothiazole and macrocyclic lactones was found in trichostrongylids on a number of sheep farms (Traversa et al., 2007). In addition one case of benzimidazole resistance has been reported in Trichostrongylus colubriformis on a goat farm (Cringoli et al., 2007). In the southern regions of Italy sheep are kept for milk production with anthelmintic treatments usually being given only twice per year to lambs (Cringoli, personal communication, 2013) and adults being left untreated during lactation (Cringoli et al., 2008, Cringoli et al., 2009). Since these practices ought to leave abundant helminths in refugia for susceptible genotypes, and this is believed to be the most important issue in the development of anthelmintic resistance (Van Wyk, 2001), there should have been little development of resistance on farms using this system.

In the present study the presence of anthelmintic resistance was investigated on 54 farms using the faecal egg count reduction test (FECRT) following the recommendations of Coles et al. (1992) on flocks of sheep using four groups of anthelmintics (benzimidazoles, levamisole, ivermectin/moxidectin and monepantel) and the FLOTAC technique having a sensitivity of 2 eggs per gram of faeces (Cringoli et al., 2010). The aim was to determine whether management practices in this region have allowed the maintenance of anthelmintic efficacy.

Section snippets

Study area

The study was conducted in the Campania region of southern Italy. In this area, sheep farms are widely distributed with an average area of approximately 50 ha. The area is mainly used for cereal production but small pastures occur on upland areas that are unsuitable for cropping.

Study farms and animals

Trials were conducted between 2008 and 2011 on 54 sheep farms.

Dairy sheep farms were randomly selected throughout the region and the selection was mainly driven by the availability of the farmer. The animals used for the

Results

The genera of nematodes present (minimum and maximum percentages in each treatment group) at the time of treatment were: Trichostrongylus (68.9–80.4%); Teladorsagia (11.6–16.3%); Oesophagostomum/Chabertia (2.7–11.2%); Haemonchus (1.9–7.4%); Cooperia (0.6–2.6%) and Bunostomum (0–0.2%). There was no significant variation of percentages in relation to year, whereas some variation was found in relation to the period of sampling, especially regarding Teladorsagia that showed the highest prevalence

Discussion

GI nematode infection (caused by different genera of nematodes, e.g. Teladorsagia, Haemonchus, Trichostrongylus and Oesophagostomum) remains one of the main constraints to small ruminant production in southern Italy (Musella et al., 2011, Dipineto et al., 2013) and so maintenance of anthelmintic efficacy is important to ensure high levels of production and animal welfare.

The present data suggest that anthelmintic resistance is rare in southern Italy and supports the idea that with correct

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

LR – participated in the study design and prepared the manuscript. ERM – performed the statistical analyses. AB – carried out the field studies. GCC – conceived the study and participated in its design and helped to draft the manuscript. CG – conceived the study and participated in its design and coordination. All authors read and approved the final manuscript.

Acknowledgements

Part of the research leading to these results has received funding from the European Union Seventh Framework Programme FP7 – KBBE-2011-5 under grant agreement n° 288975. The authors would like to express sincere appreciation to the staff of the CREMOPAR (Mirella Santaniello, Maria Elena Morgoglione, Ida Guariglia and Mario Parrilla) for their dedication to the laboratory analyses.

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The maintenance of anthelmintic efficacy in sheep in a Mediterranean climate

Abstract

Introduction

Section snippets

Study area

Study farms and animals

Results

Discussion

Competing interests

Authors’ contributions

Acknowledgements

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