Prevalence of gastrointestinal nematodes and efficacy of commonly used anthelmintics in different sheep breeds in Areka Agricultural Research Center, Areka, Ethiopia

Tewodros Getachew, Yimer Muktar¹, Negesse Mekonnen¹ and Fitsume Tesma

Areka Agricultural Research Center, Areka, Ethiopia
yimermktr21@gmail.com
¹ Haramaya University, College of Veterinary Medicine, PO. Box 138, Dire Dawa, Ethiopia

Abstract

A combination of cross-sectional and experimental study was conducted from December 2014 to January 2015 with the objectives of determining the prevalence of gastrointestinal nematodes and evaluating the efficacy of commonly used anthelmintic drugs in different sheep breeds in Areka agricultural research center sheep breed improvement farm, Wolayita, Southern Ethiopia. Prevalence study was conducted on the total of 229 sheep on station, belonging to 3 different breeds and the fecal egg count reduction test (FECRT) was used to evaluate the efficacy of anthelmintics. For the anthelmintic efficacy trial, a total of 72 sheep; 24 sheep for each breed were selected based on their higher fecal egg count (FEC) (>150 eggs).The sheep were randomly assigned in to four groups for each breed. Anthelmintics tested were Albendazole, Tetramizole and Ivermectin for each group of sheep breed.

From the total 229 different sheep examined, the overall prevalence of one or more gastrointestinal parasites was 86.6%. Individual breed prevalence was 90% for pure dorper, 92.9% for cross bred and 84.2% for local indigenous breed Predominant worm species were strongyle (71.9%), Trichuris (1.5%) and 26% of the positive specimens were harboring multiple worm species. Evaluation of the efficacy of anthelmintic by using FECRT revealed that Ivermectin and Albendazole did show resistance while Tetramizole was 100% effective against parasite treatment in all sheep breeds. Therefore the farm should practice strategic deworming system to reduce the problem of anthelmintic resistance and more controlled experimental trials that consider different season, agro ecology and using more sensitive methods like egg hatch and larval motility assay with varieties of anthelmintic brands to complement and support this finding.

Keywords: Albendazole, fecal egg count reduction test, Ivermectin, livestock, Tetramizole, parasite, small ruminant

Introduction

Livestock keeping is one of the most essential, complex and diverse subsectors of the world agriculture and a primary means of escaping poverty in rural area. Sheep production is a major component of the livestock sector in Ethiopia owing to the large population of 25.5 million head out sheep of which about 73.57 % are females and 26.43 % are males (CSA 2013). At the smallholder level, sheep are the major source of food security serving a diverse function including cash income, savings, fertilizer, socio-cultural functions. Sheep are particularly important for the pastoralist/agro pastoralist and for farmers in the sub-alpine highlands where crop production is unreliable.

Sheep are also important foreign currency earners accounting for 34% of the live animal exports and currently contributing to the livelihoods of an estimated 80% of the rural population (CSA 2013). However, the full exploitation of this huge resource are constrained by a combination of factors such as poor genetic potential, traditional system of husbandry and managements well as the presence of numerous diseases (Mtenga et al 1994).

Small ruminants reared under intensive and extensive production systems are extremely susceptible to the effects of wide range of endo-parasites which were reported to equivalent to the combined effects of other ill health problems (Biffa et al 2006; Melaku et al 2013). Gastrointestinal nematodes are one of the most important causes of losses in productivity of sheep and goats in Ethiopia (Tembely et al 1997; Abebe and Esayas 2001).

Surveys carried out in some parts of Ethiopia on prevalence of helminthes parasites showed very high prevalence of gastrointestinal (GI) parasites. Published works by (Muktar et al 1991) and (Deressa 1998) in Sheno (Abebe and Esayas 2001) in Ogaden (Regassa et al 2006) in Bako (Sissay et al 2006) in Haramaya (Kumsa and Wosene 2006) in Ogaden have showed a higher prevalence rate of GI helminthes in sheep. To improve this problem the chemotherapeutic use of anthelmintics will remain the mainstay of nematode control program (Taylor et al 2002). But one of the major problems related to the use of chemotherapy is the development of resistance to anthelmintic drugs (Waller et al 1997).

There is no anthelmintic use policy in the country as a result misuse and smuggling of anthelmintics in many forms like illegal trading in open markets and irrational administration is a widespread practice. In addition, no method is in use that can preserve and maintain the efficacy of anthelmintics or delay and prevent the emergence of anthelmintic resistance (Kumsa et al 2010).

Anthelmintic resistance in sheep is a global problem (Kaplan and Vidyashankar 2012; Chandrawathani et al 2004; Sangster and Gills 1999; Papadopoulos 2008; George et al 2011). Some studies conducted in different parts of Ethiopia such as (Chaka et al 2009) in Adami Tullu, (Asmare et al 2005; Kumsa et al 2010; Shiferaw and Asha 2010) in Southern Ethiopia, (Daniel 1998) near Addis Ababa, (Sissay et al 2006) in Haramaya, Ethiopia and (Melaku et al 2013) in North Gondar showed the presence of anthelmintic resistance of varied degree.

Despite the widespread misuse, intensive use and huge circulation of anthelmintic drugs in legal and illegal markets is rampant and there is no documented report on the efficacy of commonly used anthelmintics to control gastrointestinal nematodes in dorper sheep breeds and their crosses in Areka agricultural research center farm. Therefore, the objective of this study was to determine the prevalence of gastrointestinal nematodes and to evaluate the efficacy of commonly used anthelmintic drugs used in sheep at Areka agricultural research center.

Materials and methods

Study area

The study was conducted at Areka agricultural research center; Mente Dubo sheep breed improvement sub-station. Areka research center is placed in SNNPR in Wolaita zone which is located 300 km far from Addis Ababa, the capital of Ethiopia. Its altitude ranges from 1650 to 2980 m.a.s.l. It receives an annual rainfall ranging from 1000 - 1200 mm and an annual temperature range of 25-35°C. The area is categorized under mid land agro-ecological climate. At this time there are total of 229 different breed of sheep in the station.

Study animals and management

The study animals comprised with pure dorper, cross breed (dorper with indigenous) and indigenous sheep kept on one large farm which practiced indoor management system on Areka agricultural research center breed improvement farm. The animals shared the same watering point during day time and housed in pens during night in the farm in some cases the animals are housed in specially constructed buildings. The production system was based on indoor system of practices and no controlled mating, breeding occurring year round with two lambing cycles a year for many ewes. The history of the farms indicated that all animals received regular treatments with anthelmintics twice a year at the beginning and end of the long rainy season. The records available indicated that the types and sources of anthelmintics used on the farms included mainly Albendazole and Ivermectin for sheep.

Study design and methodology

The study was conducted using a combination of cross-sectional and farm-based experimental studies (anthelmintic efficacy test).

Cross sectional study

The cross-sectional study was carried out to determine the prevalence of gastrointestinal parasites in the farm in all breeds, which were kept under indoor farming system using purposive sampling method. Fecal specimen was collected directly from the rectum of the study animals and subjected to coprological examination using standard fecal examination techniques (Shah-Fischerand and Say 1989) and eggs of the different nematode parasites were identified on the basis of morphological appearance and size of eggs as described by Van Wyk and Mayhew (2013).

Modified Macmaster egg counting techniques:

Samples for parasite eggs were subjected to modified Macmaster egg counting techniques to quantify the parasite burden as described by Coles et al (1992). Depending on the degree of GI helminthosis, results of each specimen were categorized as low, moderate and severe for strongyle type nematodes based on (Shah-Fischerand and Say 1989)

Experimental design

After doing the fecal egg count (FEC) of Strongyle type eggs, subsequently, 109 sheep of which 40 sheep (10 in each group) for pure breed, 36 (9 in each group) for crosses and 32 (8 sheep in each group) for local breed sheep were selected which had EPG counts above 150 and did not receive anthelmintic treatments within the last 12 weeks were identified. The sheep were randomly assigned in to four treatment groups for each breed. The first group was treated with Albendazole, the second with Tetramizole, the third with Ivermectin, the fourth group was left untreated (control group). Each sheep was weighed with a scale and treatments were given based on registered label dose rate recommended by the manufacturers. Albendazole 300 mg was given at the rate of 7.5 mg/kg of body weight and Tetramizole 600 mg at 15 mg/kg body weight all being administered orally using a bolus applicator calibrated for this purpose. The Ivermectin (1%) was administered based on 0.2 mg/kg (1.0 ml/50 kg) rate by subcutaneous route with hypodermic syringes and no treatment was administered to the control group. The details of the drugs used in the tests are presented in Table 1.

Anthelmintic efficacy test

Individual sheep fecal nematode egg counts for each breed and for each treatment group were done based on 5 g of faces collected from each animal in a group on day 0 (day of treatment) before treatment and again on day 12 to 14 after treatment according to Coles et al (1992).The fecal egg count reduction tests (FECRT) were conducted and the efficacies of Albendazole, Tetramizole and Ivermectin were tested and interpreted according to the guideline provided by World Association for the Advancement of Veterinary Parasitology (WAAVP) recommendation (Coles et al 1992). The fecal nematode egg count reduction percentage (FECR%) was determined by using a formula: FECR% = 100 × (1 - Mt/Mc); Where Mt and Mc are the arithmetic mean EPG in the treated (t) and untreated control (c) groups at days 12 to 14 post treatment according to method described by Coles et al (1992) and Coles et al (2006)

Data Management and Analysis

Data were recorded in Excel spreadsheet and descriptive statistics were generated to establish the prevalence of nematode infection in the farm using STATA.11. P-value less than 0.05 were used to determine the level of significance. The efficacy of anthelmintics was evaluated based on the reduction in fecal nematode egg counts (FECR %). Calculations of the arithmetic means, percentage of reduction between pre- and post-treatment fecal nematode egg outputs and 95% upper and lower confidence limits for the reduction were conducted according to the method described by Coles et al (1992) and Coles et al (2006) and using a computer program, RESO (Anonymous 1990). Anthelmintic resistance was declared to exist when the FECR% was less than 95% and the lower 95% confidence limit for the reduction was less than 90%. If only one of the two criteria was met, resistance was suspected (Coles et al 1992).

Results

Of the 229 sheep examined, about 88.6% were found to harbor one or more GI parasite species. The prevalence of parasites infestation were not significant among the different sheep breeds (P=0.18) Table 2.

From 203 positive specimens, Strongyle type (71.9%), Trichuris (1.5%) and mixed infestation (26.6%) were the most predominant nematodes species (Table 3).

This study did show that parasite burden was light in cross and local breed type of the study animals. Pure breed sheep were found to harbor heavier parasite load than cross and local breeds of sheep (Table 4)..

Fecal Egg Count Reduction Test (FECRT):

Evaluation of the efficacy of anthelmintic based on breed revealed that the percentage reduction of fecal egg counts (FECR %) after treatment with Ivermectin was 51.76%, 87.65% and 75.86% in in pure dorper, crosses and local breed sheep, respectively. A treatment with Tetramizole was observed to be fully effective with 100.0% fecal nematode egg count reduction based on post-treatment fecal sample analysis in both crosses and local breed sheep while 98.56 % was observed in pure dorper sheep as shown in Table 5.

Fecal Egg Count Reduction Test (FECRT)

 The results of the FECRT based on treatment group for each anthelmintic are shown in Table 6. Percentage reduction in fecal egg counts and their confidence limits in the efficacy evaluation of Tetramizole (99.6%) revealed that were effective from clinical cure point of view whereas, Albendazole (90.1), and Ivermectin (84.4%) both were not effective.

Discussion

The present work revealed over all higher prevalence rates (88.6) of GIT nematode and the two main species of nematodes namely Strongyles, trichuri were found to be the most prevailing on the farm. The higher prevalence of parasites could be due to the fact that sheep could have frequent exposure to the same communal grazing land that causes contamination of pasture with the study farm. the finding of this work was comparable with the result of Niguse et al (2014) who reported a prevalence of 86.3% in Jijiga, Ethiopia, Abebe and Esayas (2001) 95.6% in Eastern part of Ethiopia and (Maichomo et al 2004), 80.0% Southwestern Kenya, respectively. On the other hand, the present result was higher than the findings of Regassa et al (2006); Nigatu (2008); Terefe et al (2013); Lemma and Abera (2013) and Dagnachew et al (2011) who reported a prevalence of 50.2% in Western Oromia, 58.18% Awi Zone of Ethiopia 72% in Bedelle, 41.49% in Dembia and 46.07% in Gondar, Ethiopia, respectively.

The species of helminthe recovered during this study were also reported by Abebe and Esayas (2001); Nigatu (2008); Shimelis et al (2011); Maichomo et al (2004) and Waruiru et al (2005). Mixed infections with more than one parasite were common (26.6%) in the current study. This finding concur with the report of Ayalew (1995) who showed 71% of sheep in Kembebit district, North-West Shoa, and Melaku et al (2013) (15.6%) in Gondar town, Northwest Ethiopia harbor one or more species of helminthes, with strongyle type being the predominant group in all breed but more higher in local breed sheep. According to Tesfaye (1998) in Kelala district of northern Ethiopia, 28.6% of the sheep populations studied were reported to be infected with two or more species. In the present study, the prevalence of GI parasites did not showed significant association with breed of sheep. The absence of association between breed and prevalence suggest that all sheep breed, pure droper, exotic and local sheep have equal chance of infection if they are exposed to the same contamination level.

The mean eggs per gram (EPG) showed that 49.8% of the sheep were lightly infested, 15.8% moderately infested and 34.5% heavily infested. This result was different from the result of Lemma and Abera (2013) who reported that 30.04% of the sheep were lightly infested, 40.34% moderately infested and 29.62% heavily infested. This difference could be due to the difference between the management and production system of examined animals and geographical and environmental location of the study area.

Fecal examination for the presence of parasite eggs in the pre-treatment fecal samples revealed that strongyle (69%). The result is higher than the report of Shimelis et al (2011), with 37.63% of strongyle eggs in Gondar but lower than the result of Lemma and Abera (2013) who reported 7.4% strongyles in Asella. The prevalence of Trichuris in the current study was (1.5%) that was lower than Lemma and Abera (2013), Regassa et al (2006) reported that the prevalence of Trichuris egg were 3.7% in Asella and 4.5% in western Oromia.

Estimating the status of anthelmintic resistance is perhaps the most important step in establishing and maintaining effective parasite control of nematode parasites in livestock, especially for small ruminants. In this study, Anthelmintic efficacy tests were conducted using three brands namely; Albendazole, Ivermectin and Tetramizole commonly available on the local markets. Regarding, the efficacy of anthelmintic based on the different sheep breed, the results of the FECRTs in the entire sheep breed showed that similar trend as the profile of the treatment group, anthelmintic resistance was not present for Tetramizole while resistance was present for the case of Albendazole and Ivermectin in all sheep breeds.

The results of the fecal egg count reduction tests (FECRT) both based on different sheep breed as well as on treatment group showed that the occurrence of resistance to treatments with Albendazole (90.05%) and Ivermectin (84.44%) of nematode egg reduction, based on the interpretation of the result according to guideline provide by World Association for the Advancement of Veterinary Parasitology (WAAVP). In contrast, treatments with Tetramizole revealed susceptibility with (99.64%) of reduction of nematode egg in the post-treatment fecal analysis. This result was fairly in agreement with the findings reported in anthelmintic efficacy tests of similar brands of drugs in Horro sheep in Western Oromiya, Ethiopia (Aga et al 2013).

However, the results recorded in the present study were inconsistent with the findings reported in North Gondar by Melaku et al (2013), in Eastern Ethiopia (Sissay et al 2006) in the Wolaita (Southern Ethiopia) Sheferaw and Asha (2010); Terefe et al (2013); Niguse et al (2014), in Cuba Arece et al (2004) in which susceptibility to Albendazole and, Ivermectin were recorded. The discrepancy between the current and previous study might be associated to high frequency of anthelmintic treatment these of the two drugs against nematode parasite in the study area. This idea was well explained by (Magona and Musisi 2002) utilization of limited group of drugs for a long period at high frequency may favor the development of resistance. Moreover sheep raisers do not have any idea on anthelmintic rotation (Niguse et al 2014) that favors anthelmintic resistance.

The present study revealed that the percentage reduction of fecal egg counts (FECR %) after treatment with Albendazole was (90.05%) with the treatment group however, it had showed different (FECR %) were recorded in different breeds of sheep studied. In the current study, Albendazole was found to show resistance in treatment efficacy of nematode parasite this result was agree with the report of Aga et al (2013) in Horro sheep in Western Oromiya, Ethiopia Sissay et al (2006) in Eastern Ethiopia, Asmare et al (2005) in Southern Ethiopia, Kumsa, and Abebe, (2009) from Hawasa, Even worse in India, Hisar University farm (Singh et al 2012). However, our finding was in disagreement with the report of Sheferaw and Asha (2010); Aga et al (2013); Sibhatu et al (2011); Terefe et al (2013); Melaku et al (2013) who reported the effectiveness of Albendazole against treatment of nematode parasite with percent of reduction in 99.34%, 98%, 100%, 96%, 99.08%, respectively. The difference of the current and the previous studies in the efficacy of Albendazole against nematode treatment might be attributed to several factors such as poor quality drugs, continuous under dosages treatments at the sheep dose rate by farmers due to low bioavailability in sheep, misuse and inappropriate treatment by owners. Such factors have been also suggested to contribute to lower efficacy (Papadopoulos 2008; Chandrawathani et al 2004; Saeed et al 2007).

Tetramizole had a very good efficacy in reducing gastrointestinal nematodes with percent reduction of 98.59 % in pure dorper sheep and 100% in both crosses and local sheep. This is in agreement with the result of Terefe et al (2013); Sibhatu et al (2011); Niguse et al (2014); Sheferaw and Asha (2010) and Aga et al (2013) who reported the effectiveness of Tetramizole with percent of reduction of 98.5%, 100%, 100%, 100% and 100%, respectively. On the other hand this result is different from the study of Melaku et al (2013) that revealed the lowest efficacy of Tetramizole with 74.29%percent of reduction.

Ivermectin was not effective in reducing fecal egg count in the current study in all breeds of study sheep. This finding was in agreement with the result of (Kumsa and Abebe 2009), Melaku et al 2013), and (Singh et al 2012) who reported lower efficacy of Ivermectin in sheep. However, this result was in disagreement, (Arece et al 2004) who reported a 100% efficacy of different formulations in Cuba, This may be related to the difference in the frequency and ways of utilization of the drug among localities. Even more, Ivermectin had relatively lower efficacy because Ivermectin were quite commonly used in the study farm .Furthermore, the differences of the efficacy of those tested drugs from other studies could be due to the difference in the frequency, dosage, misuse of drugs and ways of utilization of the drugs among the sheep on station and at farmers hand in addition to the difference study locations. This idea further explained by Aga et al (2013); Sissay et al (2006) indiscriminate use of drugs available through black markets may also impose drug failures due to under dosing or inappropriate treatments in general.

Conclusions

• This study revealed that GI nematodes in different sheep breeds especially Strongyle types, were highly prevalent in the farm.
  
  
• Prevalence of gastrointestinal nematodes had no significant association with sheep breed group, however, EPG count showed stastically significant association with the severity of infection to the breed group, that pure breed sheep were heavily infected than the other breed compared.
  
  
• The efficacy trial showed that Tetramizole was by far the most effective in reducing fecal egg output, while Ivermectin and Albendazole had showed resistance against nematode parasite.

Acknowledgements

We would like to forward our appreciation to Wolaytasodo Regional laboratory staff especially parasitology team and animal science case team for their cooperation to accomplish this work and Southern Agricultural Research Institute and Areka agricultural research center for their cooperation in using the animals for this research.

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Received 26 March 2016; Accepted 23 May 2016; Published 2 June 2016

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