Introduction
The total livestock population in Ethiopia estimated in 2012 indicates that the country is home to about 54 million cattle, 25.5 million sheep, and 24.06 million goats. Of the total cattle population, 98.95% are local breeds and the remaining are hybrid and exotic breeds; 99.8% of the sheep and nearly all goat population of the country are local breeds [1], which places Ethiopia first in Africa and ninth in the world in terms of total stock. The high stock number, however, does not lead to higher exports or export earnings for live animals or meat. Ethiopia’s annual exports of cattle and sheep meat were valued at USD 79.13 million in 2012 [2], while small ruminants are an important source of income and employment for many people globally, especially in rural areas of developing countries [3].
Small ruminants are produced under two major production systems; the sedentary mixed crop livestock production system and the nomadic pastoral or agro-pastoral production system [4]. They are raised for the production of milk, meat, leather, hair, wool, and manure [5]. The rich potential of the small ruminant sectors was not efficiently exploited due to several constraints including malnutrition, inefficient management, and diseases [6,7]. In this regard, diseases due to parasites take the lion’s share in limiting the productivity of these animals all over the world. This is especially true in many tropical and subtropical regions. Small ruminants under intensive and extensive production systems are extremely susceptible to the effects of a wide range of helminths [7].
Gastrointestinal helminths (GITs) have a disastrous impact in suppressing the performance, both in terms of production and reproduction of small ruminants [8]. It is prevalent in developing countries, mainly due to warm temperatures, in association with poor management practices and inadequate control measures [9]. This disease is caused by a range of internal parasites including roundworms, tapeworms, lungworms, and flukes [10]. Helminth parasites of small ruminants are ubiquitous in all agro-climatic zones of Ethiopia with prevailing weather condition that favors their survival and development [11]. Specifically, GI parasites are one of the main constraints to small ruminant production in temperate countries [12].
There is greater variation in the prevalence and geographical distribution of helminth infection in small ruminants in Sub-Saharan Africa. Helminths generally spend part of their life cycle outside their definitive host (such as sheep and goats), either on the ground, on grass, or within invertebrates such as snails, insects, or earthworms. Temperature, rainfall, and type of soil determine the occurrence of a given species. However, helminth control strategies for one geo-climatic region and farming systems may not be necessarily appropriate for all farming systems and agro-ecological zones due to differences in climatic and management factors [13]. Various risk factors play an important role in the onset of GIT parasite infections such as host and environment. Environmental factors include agro-ecological conditions and animal husbandry practices such as housing systems, deworming intervals, and pasture management; these largely determine the type, incidence, and severity of various parasitic diseases [14,15].
Other risk factors such as the host species, sex of the animal, age, body condition, breed/genotype, parasite species, and intensity of the worm population have an effect on the development of GI parasitic infections [16,17].
Ethiopia is among the sub-Saharan African countries where small ruminant production and productivity are affected by diseases, inadequate nutrition, and poor management systems [18]. Several studies in different parts of Ethiopia [11,19–22] indicated that GI parasites are one of the major problems causing morbidity, production loss, and mortality of small ruminants. When comparing the GIT prevalence of the study areas with other current findings of our country, Teshome et al. [23] reported 63.6% in Borana Lowlands, Southern Oromia, Ethiopia, relatively in line and lower than Sebro et al. [24] who reported 74.41% in An-Lemo, Hadiya Zone Southern, Ethiopia, and from another country, Ananda and Pradeep [25] who reported 68.75% in and around Shivamoggaa district, India.
However, helminth control strategies for one geo-climatic region and farming systems may not be necessarily appropriate for all farming systems and agro-ecological zones due to differences in climatic and management factors [26]. The consequence of risk factors of GI helminths is a major problem almost in different parts of Ethiopia. The rise of GI tract helminths problems in our country is due to the lack of sanitation, insufficiency of veterinary services at kebele levels, lack of community awareness, and lack of strategic control and prevention techniques; there was no research conducted on the prevalence of these parasites in the selected study area.
Therefore, the objective of this study was:
- To determine the prevalence of GI helminths in sheep and goats and its associated risk factors.
- Genera identification of GIT helminth infecting sheep and goats.
Materials and Methods
Description of the study area
The study was conducted in the Oromia regional state in and around Kulubi town from November 2018 to May 2019. Kulubi is located 453 km east of the capital city Addis Ababa and 48 km south of Dire Dawa city. The area is located at 9.4261567° latitude and 41.681815° longitude with an elevation of 2,417.54 m above sea level. The climate is warm and temperate in Kulubi. When compared with summer, the winters have much more rainfall. The district’s average annual rainfall ranges from 600 to 1,200 mm. The average precipitation ranges from 245 to 1,400 mm. In Meta district, Kulubi is one of the two administrative towns. In Meta Woreda, there are about 200,747 cattle, 38,322 sheep, 190,837 goats, 428 horses, 28,665 donkeys, 115 Mules, 2,418 camels, 185,652 poultry, and 2,580 different types of bee hives. The total population of Meta district is 200,686 of which 94,978 were men and 105,708 were women. There are three agro-ecological zones, namely, lowland (28.2%), mid-land (43.6%), and highland (28.2%) with a temperature range of 12°C–35°C. Farmers in the vicinity of Kulubi town use a mixed crop and livestock farming system (Fig. 1).
Figure 1.
Map of Meta Woreda where the studies were conducted.
Study population
Small ruminants in the study area are kept under a traditional extensive system by most of the families. Most families maintain one to four sheep and goats. During working time, both sex and age group of sheep and goats found in the selected seven peasant associations that share a common grazing in pasture fields were targeted for the study. According to Kumsa et al. [27] those animals with the age of less than 1 year were considered as young while those greater than or equal to one were considered as adults according to the classification of age groups. In addition, the categorized age groups depend on the size of feces that were small as young and medium and large as adults.
The body condition scores were determined according to Pant et al. [28] and were grouped as poor, medium, and good. Likewise, the body condition score was measured by external symptoms; especially in these studies, rib count was used for measurements: poor: when seven ribs were counted, medium: when three ribs were counted, and good: when no ribs were visible during inspection. In addition to these, for sheep species, the spines of vertebrae were symmetrically inspected.
Sampling method and sampling size determination
A simple random sampling system was conducted to collect the fecal samples from individual study animals. Since there was no record of previous prevalence in the study area, the sample size was determined by taking 50% expected prevalence using the formula described by Thrusfield and Brown [29]. Accordingly, a sample size of 384 (198 each for sheep and 186 goats) was considered for the study.
where
N=required sample size;
Pexp=expected prevalence;
d=desired absolute precision; and
1.96=z-value for 95% confidence interval.
Study design
A cross-sectional study was carried out from November 2018 to May 2019 to determine the prevalence and to identify genera of GI tract helminths from fecal samples collected from sheep and goats in and around Kulubi town and to identify the parasitic fauna circulating in the study area.
Fecal samples taken for laboratory procedure
Fecal samples were collected directly from the rectum of each animal during the experimental epidemiology with 10% formalin as a preservative into a universal bottle and transported to the Haramaya University Parasitology Laboratory to determine the presence or absence of parasites. Laboratory techniques such as qualitative techniques (flotation and sedimentation techniques) were utilized for separating the eggs of the parasitic agents. The collected fecal samples were processed in the laboratory and examined under 10× magnification to determine the characteristics, morphological features, granular contents, including their orders in the presence or absence of operculum at either or both sides, and the types of helminths based on color, shape, and size variation due to difference in specific gravity of parasites eggs. In the parasitological techniques, saturated sodium chloride (with specific gravity of 1.2) was used as flotation fluid for nematode eggs and methyl blue stain for differentiation of trematode eggs; since methyl blue stain has greater specific gravity than flotation fluid, it sediments rather than float on the prepared sample.
Data analysis
The data collected were organized and entered into a Microsoft Excel spreadsheet and then analyzed using Statistical Package for Social Sciences version 17. Descriptive statistics was employed to compute the frequencies of each variable with the results. Pearson’s chi-square was utilized to assess the presence of an association between independent variables (sex, age, species, and body condition) of animals with results. A statistically significant association between the variables was considered to appear if the computed p-value was less than 0.05 (p < 0.05).
Results
In the present study, a total of 384 small ruminants (198 sheep and 186 goats) were examined for the prevalence of GIT helminths, and then the mixed infection of GIT helminths was drawn out during the coprological examination. Based on the coprological examination, there was an overall prevalence of 58.9% (226/384) for GI helminths in both sheep and goats (Table 1).
In the study area, the prevalence of GIT parasites in male and female animals was 57.38% and 60.2%, respectively. This shows that the GI tract helminth infection was more prevailing in females than males. Statistically, there was no significant difference (p > 0.05) in the prevalence of helminth parasites between male and female animals (Table 2).
In the study area, the prevalence of GIT parasites in young and adult small ruminants was 72.5% and 53.45%, respectively (Table 2). This shows that the GI tract helminth infection was more prevailing in younger ones than adults. A statistically significant difference was recorded (p=0.001) in the prevalent parasite infestation between young and small adult ruminants.
With regard to species, the prevalence was higher in sheep (59.09%) when compared to goats (58.6%) and there was no significant difference (p > 0.05) in the prevalence of these parasites between the two species (Table 2). This means that the prevalence is comparable between the two host species.
In the present study, the prevalence of helminth parasites was higher in small ruminants with poor body condition (75.44%) followed by medium body-conditioned animals (56.58%) and good body-conditioned animals (54.54%). Based on the statistical analysis, there was a significant difference in the prevalence of helminths between the three body conditions (Table 2).
The results of the coprological examination in both sheep and goats have also shown the presence of several classes of GIT helminths in the two phyla of helminths. Accordingly, in goats, among the phylum of helminths and the three classes of helminths, seven genera of GIT helminths were determined, namely, genus Fasciola, genus Trichostrongylus, genus Strognyloides, genus Trichuris, genera Strongyle, genus Paramphistomum, and genus Nematodirus, while in sheep, all the genera listed in the goats were present except genus Paramphistomum and genus Nematodirus. From the nematode helminths, genera Strongyle accounts for the highest from the other genera in both species of animals, while Nematodirus eggs appear only in goats. In sheep, among class trematode, genus Fasciola was quite prevalent compared with the other genera in this group. Class cestode parasite egg was not observed in both sheep and goats in the study areas. This shows that all the helminth parasites were more prevalent in the sheep than in the goats (Table 3). (Fig. 2 and 4) Mixed helminth eggs were noticed in some of the slides examined beside the single type of helminth eggs, with an overall prevalence of 10.6% (21) in sheep host species. Among these, genera Strongyle and genus Trichuris appeared most of the time, with an overall prevalence of 4.54% in sheep-host species including zero prevalence in goat-host species (Fig. 3).
Table 1.
Assessment of overall prevalence of parasitic infestation in relation to sheep and goats by types of helminths.
| Types of helminths | Sheep (N=198) | Goats (N=186) | Total (N=384) | |||
|---|---|---|---|---|---|---|
| Positive | Prevalence (%) | Positive | Prevalence (%) | Total positive | Overall prevalence (%) | |
| Nematodes | 111 | 56.06 | 79 | 42.48 | 190 | 49.5 |
| Trematodes | 6 | 3.03 | 30 | 16.12 | 36 | 9.4 |
| Total | 117 | 59.09 | 109 | 58.6 | 226 | 58.9 |
N=Number of animals.
Table 3.
GIT parasite eggs identified by coprological examination in the study area.
| Parasites | Sheep (N=198) | Goat (N=186) | Total (N=384) |
|---|---|---|---|
| Fasciola | 3.03% (6) | 8.06% (15) | 5.47% (21) |
| Trichostrongyles | 10.6% (21) | 8.6% (16) | 9.63% (37) |
| Strongyloides | 6.58% (13) | 3.23% (6) | 4.95% (19) |
| Trichuris | 8.08% (16) | 6.45% (12) | 7.3% (28) |
| Strongyles | 20.2% (40) | 18.8% (35) | 19.53% (75) |
| Paramphistomum | 0% (0) | 8.06% (15) | 3.9% (15) |
| Nematodirus | 0% (0) | 5.4% (10) | 2.6% (10) |
| Mixed | 10.6% (21) | 0% (0) | 5.47% (21) |
| Overall | 59.09% (117) | 58.6% (109) | 58.9% (226) |
N=number of noticed animals,=53.795, df=8, and p=0.000.
Table 2.
Prevalence of GI helminths in the small ruminants by sex, age, species, and body condition.
| Risk factor | No. examined | No. positive | Prevalence (%) | χ2 (p-value) |
|---|---|---|---|---|
| Sex | 0.315 (0.604) | |||
| Male | 183 | 105 | 57.38 | |
| Female | 201 | 121 | 60.2 | |
| Total | 384 | |||
| Age | 11.664 (0.001) | |||
| Adult | 275 | 147 | 53.45 | |
| Young | 109 | 79 | 72.5 | |
| Total | 384 | |||
| Species | 0.009 (1.000) | |||
| Sheep | 198 | 117 | 59.09 | |
| Goats | 186 | 109 | 58.6 | |
| Total | 384 | |||
| Body condition | 7.72 (0.021) | |||
| Poor | 57 | 43 | 75.44 | |
| Medium | 228 | 129 | 56.58 | |
| Good | 99 | 54 | 54.54 | |
| Total | 384 |
χ2=chi-square.
Discussion
The coprological examination in the present study revealed that the small ruminants were infested with at least one species and at most two species of parasites. The overall prevalence of the helminth parasite was 58.9%. Specifically, the prevalence of 59.09% with various GIT helminth infections was recorded in sheep, and similarly, 58.6% was recorded in goats.
The prevalence of helminth parasites in the study area was lower compared to the finding of (95.6% in sheep and 100% in goats) Abebe and Esayas [30]; (60%–80% in both species) Sissay et al. [11]; (67.7% in both species) Zeryehun [31]; (88.67% in both species) Kelemework et al. [32]; (77.8% in both species) Dabasa et al. [33]; (87.2% in both species) Ibrahim et al. [7]; (91.9% in both species) Mulugeta et al. [34]; and (87.8% in both species) Bedada et al. [35]) and higher than the results of other study in sheep and goats (53.9 in both species) [22] in Eastern Ethiopia; (49.2% in both species) [36] in Western Ethiopia; (48.21% in both species) [37] in Northern Ethiopia; and (47.67% in both species) [19] in Northwest Ethiopia. This difference in prevalence could be related to variations such as season of study, age, and stage of infestation and treatment of animals [38].
Figure 2.
Overall prevalence of GIT helminth infection in small ruminants identified in Meta Woreda.
Figure 3.
Overall prevalence of mixed GIT helminths infection only in sheep in Meta Woreda.
This difference in prevalence in different ecological regions could be further explained by the existence of favorable climatic conditions [39] that support prolonged survival of the infective larvae stage. There exists a direct relationship between moisture and the prevalence of parasitosis [40] while desiccation suppresses the development and growth of parasites [19], thereby reducing the infection rate. In addition, the variation of altitude helps to get different genera of parasite eggs; host factors that determine the susceptibly to GIT helminths and parasitic factors that give different prepatent periods to helminths for the continuation of life cycle could also be other factors.
In the present study, the prevalence of helminth parasites was somewhat higher (59.09%) in sheep than in goats (58.6%). However, there was no significant difference (p > 0.05) in the prevalence between the two animal species. This finding was in the same line with other works of Emiru et al. [41] in Southwest Ethiopia, Zeryehun [31] in Southeastern Ethiopia, Kelemework et al. [32] in Eastern Ethiopia, Derso and Shime [42] and Shime [43] in Northwest of Ethiopia, Negasi et al. [37] in Northern Ethiopia, Ibrahim et al. [7] in Western Ethiopia, and elsewhere in the world Lathamani et al. [44] in Tumkur, Khajuria et al. [45] in Jammu province, Singh et al. [46] in western Punjab, India, that higher prevalence was observed in sheep than goats.
Figure 4.
Overall prevalence of single GIT helminth infection only in goats in Meta Woreda.
The higher prevalence of GIT parasitic infections in sheep as compared to goats was probably due to their grazing behavior. As sheep graze very close to the ground, the risk of ingestion of parasitic ova is comparatively higher than the goats, as they are browsers [31,32,44,46].
In the present study, a higher prevalence was observed in young animals than in adult animals, and there was a statistically significant difference (p < 0.05) between age groups. The prevalence of GIT helminths parasite in the study area was 72.5% and 53.45% for young and adult animals, respectively, and this result was similar to other findings that reported higher prevalence in young animals than in adult animals such as Negasi et al. [37] in Northern Ethiopia, Lemma and Abera [47] in South Eastern Ethiopia, Derso and Shime [42] and Shime [43] in Northwest Ethiopia, and Teshome et al. [23] in Southeastern Ethiopia. This might be due to young animals being susceptible to different diseases including parasitic infection due to low development of the immune response to the infection, lack of adaptation, and resistance before exposure to infection, whereas adult animals are resistant and adapted to infection due to rapid response of immunity to the infection due to previous exposure of infection which remove the parasites before they get attached to the predilection sites.
In the present study, the prevalence of the parasites was found higher in female animals than in male animals. This finding agreed with other studies by Zeryehun [31] in South Eastern Ethiopia, and Dagnachew et al. [19], Tesfaye et al. [21], Derso and Shime [42], and Shime [43] in Northwest Ethiopia. This higher prevalence might be due to male animals being sold in larger numbers than in female animals, and more samples were collected from the females and female animals’ immunity may be lower than male animals during lactation and pregnancy. In addition, male animals are kept indoors for fattening purposes to fulfill household and family needs, and then the rest can be freed to communal grazing areas with females for breeding continuation to compensate the generation.
The present study showed that a higher prevalence of helminth infection was observed in poor body-conditioned animals as compared to medium and good body-conditioned animals, and there was a statistical significance (p < 0.05) between body conditions. The prevalence of helminth parasites in these studs in relation to body conditions was 75.44%, 56.58%, and 54.54% in poor, medium, and good body conditions. This finding is similar to other studies such as Lemma and Abera [47] in South Eastern Ethiopia, Tesfaye et al. [21], Derso and Shime [42] and Shime [43] in Northwest Ethiopia, Negasi et al. [37] in Northern Ethiopia, and elsewhere in the world is Lathamani et al. [44] in Tumkur. The higher prevalence of poor body conditions might be caused by malnutrition, other concurrent diseases, or current parasitic infections that lead to reduce the immune status of the animal [37] and the presence of the adult parasite inside the hosts that compete for sharing of feed for the continuation of life cycle these lead the disorder normal function and damage of the host’s organs. The poor body-conditioned animals are more exposed than the remaining body conditions due to concurrent diseases caused by either bacteria or virus microorganisms that play a great role by complicating the body functions through disordering to lead to lowering immunity of the hosts and the desire for feed by poor body conditions animals are very higher than the rest body conditions.
The current study has shown the presence of mixed infection characterized by the presence of two or more helminth genera both in sheep and goats, and this is in agreement with the findings of other researchers in the country [30,34,40,48–50]. This polyparasitism has been suggested to be an important cause of morbidity and loss of production in sheep and goats [27]. Moreover, the presence of interaction and compromization of the immune system of the host by polyparasitism has been described to increase their susceptibility to other diseases or parasites [51]. Hence, mixed infection is an important problem of sheep production in the current study area due to the use of anthelmintic drugs for fattening purposes of goat species, and other possible factors could be the number of eggs laid by female parasites and uneven distribution of parasites eggs in the feces of animals.
Finally, the constraints and limitations encountered in these study areas must be resolved in the future research intended for individuals or organizations in the prevalence of GIT parasites. The study was made only in one seasonal occurrence, was not included in all seasons, and also did not determine the burden of GIT parasites through qualitative laboratory methods; the samples were taken from Kulubi to Haramaya University by adding preservatives such as 10% formalin in the fecal sample and processed after 2 days at Haramaya University’s Veterinary Parasitology Laboratory, which made the prevalence to be less, and the significance and insignificance of the fecal samples of herds were determined through software analysis.
Conclusion
In general, the overall prevalence of GI helminth parasites in the study area indicates GI helminthosis to be an important health problem. The present study showed a considerable relation between age groups and the body condition of animals. Statically there was no significance between species of animals and sex of animals. The present study depends only on qualitative laboratory techniques and not on quantitative laboratory techniques to determine the burden degree of GIT helminths, and in the case of seasons, it is done only during the summer season. In future studies, researchers must identify all genera circulating the study areas by including fecal cultures. In both sheep and goats, the nematode parasites were the most predominant parasites followed by trematodes. The majority of sheep and goats were infected by single parasite types of infections and mixed infection was common only in sheep.
Based on the above conclusion, the following recommendations are forwarded.
- Strategic deworming of animals, when conditions are most favorable for larval development on the pasture by using broad-spectrum anthelmintics.
- Proper pasture and animal management is a key component to managing GI helminths.
- Rotation grazing is used in intervals and avoids communal grazing with other animals to avoid cross-parasite contamination.
- The role of veterinarians in giving professional advice regarding preventive and control measures against GI helminths should be prominent to prevent drug abuse.
- Effective feed resources according to the age or stage of animals from agricultural by-products, natural pastures, and browses, and appropriate nutritional supplementation programs for young, adult, and lactating animals.
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