Camel gastrointestinal helminths in selected districts of Somali regional state, eastern Ethiopia

Magan Muhomed, Berhanu Sibhat and Jelalu Kemal

Haramaya University College of Veterinary Medicine, P O Box, 138, Dire Dawa, Ethiopia.
jelaluk@gmail.com

Abstract

Camels are a sub-set of huge livestock resources in Ethiopia. Gastrointestinal helminth infestation is one of the major obstacles to growth and development that causes impaired milk and meat production, fertility and low calving rates of camels. A cross-sectional study was conducted with the objectives of estimating the prevalence of gastrointestinal helminths affecting camels and to determine the risk factors associated with gastrointestinal helminths infection of camels in Jigjiga and Gursum districts of Somali Regional State, Ethiopia. Flotation and sedimentation, and MacMaster counting techniques were used to identify the type of helminths parasites and burden of infestation, respectively.

Feacal examinations revealed an overall prevalence of 79.0%. Out of 238 examined camels, 188 shed helminth ova in their feaces. The most commonly encountered parasites were Strongyle spp. (64.7%), Strongyloides spp. (22.3%), Trichuris spp. (12.2%), Paraphistomum spp. (1.7%), Fasciola spp. (2.1%) and Monezia spp. (8.4%). Among the risk factors age was observed to be significantly associated with helminth infection (p=0.007). Animals aged 11 years and above were found to harbour heavier parasite load than animals <5 years and between 6-10 years. Other hypothesised risk factors such as origin, body condition score and sex of camels had insignificantly effect on prevalence of helminth parasites (P>0.05). There was no significant difference in the EPG count based on sex, origin and body condition score (P >0.05). The study showed that the gastrointestinal helminths are important health problems that affect the wellbeing and productivity of the camels. More emphasis should be given to appropriate prevention and control options based on detailed epidemiological study that consider parasite dynamics with in camels and the environment with seasons.

Key Words: prevalence, risk factors, faecal examination, Fafan Zone

Introduction

The one humped camel (Camelus dromedaries) plays an important role in the subsistence economy of the pastoral society of the eastern Ethiopian Somali by providing milk, meat and it is also as sole source of transportation as well as socio-cultural aspects such as prestige, compensation for blood, dowry and the like (Bekele 2002). Camels are a sub-set of huge livestock resources in Ethiopia, in which the population estimated to be over one million, inhabiting the arid and semi-arid areas of the country that constitute more than 60% of the total area and home of pastoral and agro pastoral communities (Abebe 2000).

Pathogenic diseases, poor nutrition and traditional management systems as well as lack of veterinary services have hampered their full utilization, despite the importance of dromedary in the pastoral areas where the environment is harsh and hostile (Bekele 2002). Gastrointestinal parasites (GIT) are one of the major obstacles to growth and development of animal health. Factors like constant exposure to parasitic infestation include variable geo-climatic condition, shortage of food and lack of knowledge of farmers in treating GIT parasites play an important role in proliferation of the parasites and their diseases (Durrani 1991). Numerous parasites infect camels many of whom are responsible for enteric infection (Parsani et al 2008). Camels can acquire helminths infection by grazing on infected pastures or by ingesting infective larvae with drinking water (Fowler 1996).

Camelids are affected by different types of GIT parasites. A number of these helminths are camelids specific, but some are also common to other hosts, especially domestic ruminants and wild animals (Wernery and Kadden 2002). Gastrointestinal helminthic infestation is one of the major causes of impaired milk and meat production, as well as impaired fertility and low calving rates of camels. It cause losses through morbidity and hidden effects on feed intake, efficiency of nutrient utilization and also reduce growth rate in young animals. As a result, it leads to reduction in productivity and performance of the infested animal (Bekele 2002).

Helminth infestation is very much prevalent in camel and it imposes considerable constraints on camel health and production, thereby causing economical losses to camel owners (Bekele 2002). Haemonchus longistipesis the most pathogenic enteric nematode of camels that may be associated with Trichostrongylus species infestation which may contribute to the debilitating effects of gastrointestinal nematodes (Chabra and Gupta 2006). Previous studies have shown that higher proportion of pastoralist camels were infected by one or more helminthic parasites. On the basis of faecal samples and post-mortem examination, the prevalence of helminths was estimated that 92% of the animals examined in various parts of Ethiopia were to some degree infested with internal parasites (80% with strongyleova, 10% with Strongyloides larvae and 16% with Trichuris ova). Fourteen helminths species were identified on post-mortem examination, the main ones being include: Monezia species, Stilesia avittata, Avitellina centripunctata, Trichuris globosus, Haemonchus contortus, Trichostrongylus species and Impalaia somaliensis. Mixed infections withHaemonchus, Trichuris, Cooperia, Nematodirus andTrichostrongylus species, to name a few, are the most common (Richard 1979).

Heavy helminthic infection causes significant impact in these animals resulting in high morbidity and mortality. Despite importance of camels in the subsistence economy on marginal areas of the country, knowledge on camel husbandry management and parasitic diseases control is still very unreliable and sufficient information is not available in Ethiopia. Researches that have been conducted on camel GIT helminths prevalence are very limited particularly in Fafan Zone, Somali Regional State, Ethiopia. Therefore, this study was conducted in order to assess the current status and estimate the prevalence of camel gastrointestinal helminths in selected district of Fafan Zone, identify major GIT helminths responsible for camel GIT infection and to identify associated risk factors for camel GIT parasites.

Materials and Methods

Study Area

This study was conducted from November 2015 to May 2016 in two conveniently selected districts of Fafan Zone, namely Jigjiga and Gursum districts. Fafan Zone is one of the nine administrative zones of Somali Regional State of Ethiopia (SRSE). The zonal and also regional capital, Jigjiga city, is located 630km South East of Addis Ababa. Jigjiga is situated at geographical coordinates of 9^o20’ North latitude and 42 ^o50’ East longitude, with an altitude ranging from 1,660-1,850 m.a.s.l. Fafan administrative zone, has a typical pastoral and agro-pastoral setting whereas the climate of Jigjiga and Gursum is semi-arid type which is characterized by high temperature and low rainfall. The areas have mean annual average rainfalls of 400 to 500 mm, and minimum and maximum average temperature of 17 ^oC to 31 ^oC respectively. The vegetation cover mainly includes dwarf shrubs, large shrubs and trees (such as Acacia, and Boscia species) and highly populated cacti. Livestock herding is a prevalent profession of the rural population with free range pastoralist and agro-pastoralist management as the most dominant production systems. The camel population of Fafan Zone is estimated to be at 81,221 of which 15,850 heads are found in Jigjiga and Gursum districts (LCRDB 2005).

Study Population

The study animals consisted of indigenous breeds of one humped camel ( Camelus dromedarius) reared under pastoral management system which allows free grazing, usually mixed with livestock from other villages, the animals move from feed shortage area to feed abundant areas especially during drought season. Camel of all age categories and both sexes were included for this study.

Study Design

A cross sectional study was conducted from November, 2015 to June, 2016 to estimate the prevalence and associated risk factors for the occurrence of camel gastrointestinal helminths in the study area

Sample Size Determination and Sampling Method

Sample size was determined based on earlier study (80.7%) prevalence of camel GIT parasites at Yabello district by (Demelesh et al. 2014). Then the sample size was calculated as per the method described by (Thrusfield 2005) with 5 % acceptable error and 95% confidence level. Accordingly a total of 238 animals were sampled from the study area. From selected districts three peasant associations (PA’s), (one PA’s from Jigjiga district and two PA’s from Gursum district) were chosen purposively based on their accessibility, camel population, proximity to livestock market, availability of watering points and other socioeconomic characteristics were considered in selecting the PAs. On willingness-basis 84 camels were sampled from Hadow, and 77 camels each were sampled from Fafan and Tikdam PAs. The age of studied camels was categorised into <5, 6-10 and >11 years. The age of the sampled animals was determined by dental eruption according to (Khan et al 2003). The body condition score (BCS) of sampled camels were evaluated by looking at the back and flank of camels which was latter categorized as good, medium and poor according to (Faye et al 2001).

Laboratory Investigation

Sample collection, transport and handling

Faecal samples were directly collected from the rectum using clean hand gloves and approximately 15g amount of faeces was placed into separate universal bottles. Proper dating, labelling and coding of the sample was done on the spot. Animal attributes such as sex, age and body condition score were also recorded for each camel. Collected feacal samples were immediately transported to Jigjiga Regional Veterinary Diagnostic and Research Laboratory through perfectly maintained icepack and stored there at 4 ^oC for maximum of one day until the analysis was commenced.

Coprological examination

Faecal samples were grossly visualized to determine colour, consistency and presence of adult worms or other contaminants. Qualitative faecal examination was conducted in which faecal samples was processed by applying faecal floatation and sedimentation techniques for detection of parasite eggs as described by (Soulsby 1982). Finally using McMaster counting slide the faecal egg counting (FEC) was performed to determine parasite load in the positive fecal samples as described by (Urquhart et al 1996). The EPG was classified as light, moderate and heavy infection for a count of 50 to 799, 800 to 1200 and over 1200, respectively.

Data Analysis

All collected data was entered into Microsoft excel and analysis was done using STATA 12.1. The prevalence was determined by the rate of the number of infested animals and total number of animals in the population as described by the formula of (Thrusfield 2005). Association between hypothesized risk factors like origin, age, sex and BCS was related using logistic regression. (P<0.05) was considered as statistically significant in all cases.

Results

Of the total 238 camels examined, 188 (79%, 95% CI=73.2-84.0) were observed that harbour one or more types of gastrointestinal parasites at varying levels. The data analysis conducted during the study indicated no significant association (P>0.05) between camels districts and gastrointestinal parasite infection (Table 1). However, prevalence of GIT helminths of camels in Jigjiga was slightly higher than camels in Gursum.

Of all the camels examined in the three PA's, samples from Hadow had the highest GIT helminth while Tikdam had the lowest infection prevalence. However there was no differences (P>0.05) in the prevalence (Table 2).

With regards to parasite composition, several types of parasite ova were identified during the laboratory analysis. Nematode, trematode and cestode type ova were observed with varying frequencies. The most prevalent ones were Strongyle type ova followed by Strongyloides spp. while the least abundant were Paramphistomun spp. (Table 3).

In this study mixed infestation consisting of two and three parasitic ova types were observed. The prevalence of two parasitic eggs in female camels was slightly higher than the prevalence of two parasitic eggs in males (25.5%) and the prevalence of three parasitic eggs was lower in males (2.1%) than in females (4.7%) (Table 4).

Females and males were found to be infected with a prevalence of 80.6% and 72.3%, respectively. Similarly, animals <5 years, between 6-10 years and >11 years of age were infected with significant differences (p=0.007). Animals aged 11 years and above were harboured heavier parasite load than animals < 5 years and between 6-10 years. (Table 5). Infection prevalence was slightly higher in animal with poor body condition when compared to that of medium and good body condition with no significant difference (P>0.05) (Table 5).

When the predictors with p-value less than 0.25 (sex, age) were subjected to multivariable logistic regression, only age of animals were significantly associated with gastrointestinal helminth ova status (p=0.007). Camels with 11 years and older were 18.0 (2.05-157.8) times more likely to be positive for parasite ova than younger ones (data not shown).

In this study it was shown that parasite burden was highly related to the age of the animals and had differences. There were differences in the degree of EPG between animals <5 years, between 6-10 years and >11 years (p=0.003), and animals >11 years of age were harboured heavier parasite load than animals <5 years and between 6-10 years. Both body condition and sex showed no significant association with EPG (p>0.05) (Table 6).

Discussion

According to the result of the study it was found that GIT helminthiasis is one of the main problems of camel health in the study area. The findings of this study are in agreement with the result of other researchers, that GIT helminthiasis is main problem in camel worldwide (Fadl et al 1992 and Rewatkar et al 2009). This study revealed that out of 238 camels examined 79% (188/238) of camels harbour at least one type of gastrointestinal helminthic parasites. This findings coincides with previous reports of overall infestation rate of 80.73% in Yabello (Demelash et al 2014) ,78.0% in Sokoto metropolis (Mahmud et al 2014), 75% in Nigeria (Ukashatu et al 2012), 75.1% in Iranian camels (Borji et al 2010), 75% in eastern Ethiopia (Bekele 2002) and 76.2% in Bahrain (Abubakr et al 2000). However, this finding was comparatively lower than prevalence reports of 92.4% in Nigeria (Bamaiyi and kalu 2011), 96.9% in eastern Ethiopia (Tekle and Abede 2001) and 98% in Jordan (Sharrif et al 1997). In contrast, this result was higher than prevalence reports of 26.9% in camels of Egypt (Ahmed 2014), 28.4% in the camels of the desert thal of Pakistan (Alvi et al 2013), 37.3% in camels of Faisalabad (Azhar et al 2013), 62.7% in northern Tanzania (Swai et al 2011) and 68.9% dromadaries in Nigeria (Kamani et al 2008). Relatively the higher prevalence of GIT helminthiasis of camels in the study area could be attributed to lack of improved animal health management system and lack of knowledge of farmers in treating GIT parasites.The possible explanation for the country to country variation in the infestation rate could be variations in agro-ecological conditions between countries, which favor or disfavor the survival of parasites eggs and larvae, management system and husbandry practices (Allport et al 2005; Mohamed et al 2008). Moreover the occurrence of parasite is associated with nutritional status, level of immunity, rainfall, humidity and temperature differences and season of examination on the respective study areas.

Six different types of gastrointestinal parasite ova were identified in camels. They were broadly classified as nematodes (Strongyle type ova,Strongyloides spp. and Trichuris spp.), cestode (Monezia spp.) and trematodes (Fasciola spp. and Paraphistomum spp.) according to the egg structures (Soulsby 1982; Urquhart et al 1996; Max et al 2006). Mixed parasitism involving two or more helminths was common in the present study and is in agreements with the results of other researchers (Bekele 2002; Rewatkar et al 2009; Swai et al 2011). Strongyle type nematode ova occurred in 154 of 238 camels (64.7%) examined and was the most prevalent gastrointestinal parasite encountered during the study and this is in agreement with prevalence of GIT helminths at Yabello (Kasahun et al 2014). Origin of the animals (both districts and PAs) were compared and there was no statistically significant difference between them (P>0.05). The most probable reason for this could be the similarity in microclimates of the localities.

The result of this study also showed that there was no statistically significant difference in the prevalence and intensity of GIT helminths in relation to sex (P>0.05). Although the number of examined males was lower than females, the prevalence and intensity infestation (FEC) rate was slightly higher in females than male camels. This finding concur with most of previous researcher who have observed higher rates of parasite infestation/worm burden in female hosts compared with the males (Maqsood et al 1996; Komoin et al 1999; Valcarcel and Romero 1999), contrarily Gulland and Fox (1992) found higher rate of infestation in male than females. Generally the slightly higher prevalence of parasites in female camels than male counterparts is may be due to the physiological peculiarities of the female camels such as pregnancy and parturition, which usually constitute stress factors thus reducing their immunity to infections (Wakelin 1984).

The result of this study indicated that there was statistically significant difference in the prevalence of GIT helminths in relation to age groups (p=0.007). It revealed higher prevalence in camels with 11 years and older (97.1%), followed by camels between 6-10 years (77.8%) in which camels <5 year had lowest prevalence (62.5%).This is in agreement with Demelesh et al (2014), who reported increasing rate of infestation with age of camels. The tendency of higher prevalence in older age in the present study can be associated with the increase chance of parasitic encounter along with the decrease of body immunity against infestation (Demelesh et al 2014). In contrary to this result Swai et al (2011) observed higher prevalence in 6-10 years old (70%) followed by camels >10 years old (60.5%). Regarding the relation of EPG with age there was a significant association (p=0.003) between the age and the severity of infection and this is in agreement with Kasahun et al (2014).

The study further revealed that body conditions of the animal did not show significant association with the prevalence of the GI parasites (p>0.05). This is in line with (Kasahun et al 2014). The absence of association between body condition and prevalence could be explained by the fact that loss of body condition in the study animals could be due to other factors such as seasonal change of forgeable feedstuff and the presence of other concurrent disease conditions, as the study was conducted in some of the lowland areas (Swai et al 2011).The poor body condition could also be due with the unusually severe drought that occurred during the study period. But this finding disagrees with previous reports in other livestock species (Keyyu et al 2003). Similarly, statistically insignificant differences in mean eggs per gram of faeces was observed with body condition score (P>0.05). This finding disagrees with previous findings reported by Demelesh et al (2014) and Bekele (2010) from Yabello and Borena camels, respectively, however the higher EPG count that is commonly encountered in pastoral camels could mainly be aggravated by the management system and lack of deworming practices by herd owners.

Conclusions

• The result of the present study indicated that the prevalence of gastrointestinal helminths in the study area was estimated to be 79%.
  
  
• Three general ova types of nematodes including Strongyle type, Strongyloides spp., and Trichuris spp were identified whereas Monezia spp. was the only cestode detected in the study area.
  
  
• Trematode eggs of Fasciola spp. and Paraphistomum spp. were also observed but with lower prevalence.
  
  
• It was found that only age among the considered risk factors (which in addition include body condition, sex and origin) was found to be statistically significantly associated with prevalence of camel GIT helminths. Further studies should be conducted to determine the parasite dynamics at different seasons of the year in order to recommend the best prevention strategy.

Acknowledgements

We are grateful to Livestock, Crop and Rural Development Bureau of Somali Regional State of Ethiopia for providing materials and support. We like to appreciate Dr. Abdirisak Muhamed and Mr. Eshetu Zewde, Jigjiga Regional Veterinary Diagnostic and Research Laboratory for their friendly cooperation.

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Received 6 December 2016; Accepted 15 December 2016; Published 1 March 2017

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