Prevalence of endo-parasites in donkeys and camels in Karamoja sub-region, North-eastern Uganda

Donkeys (Ass-Equus-assinus) and camels (Camelus dromedarius) in Uganda are mainly owned by low income earners and peasant farmers, mainly in the semi-arid North-eastern Uganda in Karamoja and Sebei sub-regions. The animals however, seem to receive little or relatively no veterinary care. This study was carried out in Moroto and Amudat districts, Karamoja sub-region, Uganda in March 2016. Faecal samples of 110 randomly selected camels and donkeys of all age and sex were collected directly from their rectum. The faecal samples were examined by flotation method, sedimentation technique, McMaster egg counting technique and faecal culture to identify and determine the burden of parasites in different age groups. Lungworms ovaculture revealed Dictyocaulus cameli (29.3%) of camels and Dictyocaulus arnfieldi (15.4%) of donkeys. Cestode eggs detection revealed family Anoplocephalidae which includes seven species of cestodes identifiable as eggs in faeces or as adults in the gastrointestinal tract of camels (18.3%) and donkeys (15.4%). Coccidia species included Eimeria cameli (11%) and Eimeria Leuckarti (3.85%) in camels and donkeys, respectively. Trematodes were detected in 5 camels as Fasciola gigantica. Overall, EPG count was observed for strongyles at 58.5% in camels and 42.3% in donkeys. The results of this study will provide insights into the health of donkeys and camels in Uganda and provide a way forward to their veterinary care and management for improved production and productivity.


INTRODUCTION
Donkeys and camels are subject to severe work and in bondage, working in extremely strenuous conditions, over laden, underfed and ill-used especially for draught purposes. They are sore footed, constantly burdened by parasites (Atawalna et al., 2015;Tsegaye and Chala, 2015;Ismail et al., 2016;Anvari-Tafti et al., 2013), with little or no veterinary care. An attempt to study parasitism in these species has only been recent.
Parasitic helminthes are one of the most common factors that constrain the health and working performance of camels and donkeys worldwide. Parasites cause various degrees of damage depending on the species and number present, nutritional and the immune status of the animal (Sumbria et al., 2014;  . Infection by endo-parasites in camels and donkeys are responsible for problems including poor body condition, reduced power output, diarrhea, colic, emaciation, impaired growth, poor reproductive performance, short lifespan and predisposition to other infectious diseases (Ayele, 2006;Fikru et al., 2005;Getachew et al., 2010;Yoseph et al., 2005).
The prevalence, species composition and epidemiology of helminthes affecting donkeys and camels have not been previously investigated in Uganda. Donkeys and camels are used in arid and mountain villages, both as saddle animals and for carriage. In camels and donkeys, nematodes are seen to be most prevalent, while cestodes and trematodes are less occurring (Arslan and Umur, 1998;Bakirci et al., 2004;Demir et al., 1995). Eimeria species can also be encountered (Arslan and Umur, 1998;Bakirci et al., 2004;Ozer and Küçükerden, 1992).
Nematode infection was the most prevalent challenge in these species. A heavy internal parasite burden can adversely affect the health of donkeys and camels particularly when called upon to work and as it is often the case, is undernourished and stressed (Sonja et al., 2000).
The present study was therefore designed to generate baseline data on the prevalence and species composition of helminth parasites of donkeys and camels in Uganda.

MATERIALS AND METHODS
Faecal samples were collected from Karamoja sub-region in two districts namely: Moroto: N 2° 31' 41.604", E 34° 39' 28.794" and Amudat: N 1° 47' 29.841", E 34° 54' 23.583" districts, Uganda. The study was conducted in March 2016. The camels and donkeys were classified as: infant, juvenile, sub-adult and adult. Male and female animals were sampled (Table 1). Karamoja sub-region is a semi-arid region, the livelihoods of the people depend on pastoralism. Cattle, sheep and goat are kept in large numbers for meat, milk, blood, dowry, prestige. Donkeys and camels are kept for draught power, meat and milk. Faecal samples were collected directly from the rectum of the animal using a gloved hand, into polyethene bags, labeled using details such as source, age, sex, species and general condition of animal for easy identification, cold chain was maintained in the field and the samples were hurriedly taken to the parasitology laboratory for analysis to avoid larval development.
Samples were kept in refrigerator at 4°C if immediate processing was not possible, but it had been processed within 48 h or as soon as possible. Direct faecal smear, sedimentation and floatation techniques were the utilized parasitological techniques to identify the eggs in faeces and examined microscopically (10 and 40×) for presence of parasite ova following their procedures (Forety, 2001). Identification of the eggs was made on the basis of their morphology (Soulsby, 1982). Quantitative faecal examination was performed by using McMaster technique (Gordon and Whitlock, 1939) to determine the number of egg per gram of faeces (EPG) and performed according to the procedure described by Urquhart et al. (1996). Faecal culture using Baermann technique to determine lungworm larvae, Dictyocaulus arnifieldi and Dictyocaulus cameli was also undertaken. Level of infection was extrapolated from infection severity index (Soulsby, 1986) where animals are said to have mild, moderate and severe nematode infestation if their faecal egg counts are less than 500, 500-1000 and more than 1000, respectively.

Data management and analysis
The data collected from the study area was entered into Microsoft Excel spread sheet and the data was coded appropriately and analyzed using SPSS version 16 statistical software. Analysis Of variance (ANOVA) test was applied to test the statistical association existing among the risk factors such as species, sex, age and body condition scoring with the presence of the infection.

RESULTS
The total number of donkeys was 26, while camels were 82 giving a total of 108 animal samples analyzed. Coccidia reported Eimeria cameli in camels with 9 cases in camel at a mean count of 34 at a prevalence of 11%, while Eimeria leuckarti in donkeys reported 1 case with a mean count of 11.5 at a prevalence of 3.85%.

Level of infection
Animals were said to have mild, moderate and severe Ugandan camels (Camelus dromedaries) were infected with E. cameli (11%) while 3.85% donkeys had Eimeria leuckarti. It is believed that the infection of coccidia is concern mainly with young horses and donkeys, especially foals. Although, it has been reported that E. leuckarti is more prevalent among young foals and only occasionally is it detected in adult animals (Souza et al., 2009). Watering devices should be protected from faecal contamination. Diagnosis is based on clinical signs and the demonstration of high numbers of oocysts in the diarrhoeic faeces. Cystic structures containing immature oocysts occur in the intestinal mucosa. In the present study, in all the cases, no clinical signs were documented in the animals excreting E. leuckarti oocysts, while there were some doubt about the pathogenicity of E. leuckarti, diarrhea of several days duration, and acute massive intestinal hemorrhage leading to rapid death have been described in foals (Radostits et al., 2006). However, the infection is rarely evidenced by clinical signs. Difficulties in the diagnosis of coccidia infection in camels, horses and donkeys cause the parasitosis not to be diagnosed in a routine coproscopical examination.
Strongyle eggs were quantified to determine egg per gram of faeces (EPG). Strongyles were taken as a group, speciation of the nematodes by ovaculture was not done. All the camels and donkeys were in good health and body condition except one sick donkey in Moroto which was in poor body condition. For this reason, autopsy was not done and hence adult worms were not studied. Therapy and prophylaxis for all the above mentioned helminth parasites is the same as for cattle.
Veterinary health care provision in Uganda does not cater for donkeys and camels at all. No veterinary intervention for these animals in Uganda is available at all. Yet these animals are kept in arid and mountainous areas of Karamoja and Sebei sub-region in North-eastern Uganda. They are kept for milk, meat, dowry, prestige and carriage.
Mixed infections were encountered comprising of double infections or triple infections of Strongyle, coccidian, cestode, trematode and lungworms. The challenge of mixed infections exacerbates the compromised health condition of the animal which could result in debilitation and death of the animal.
The number of eggs per gram can be calculated by counting the number of eggs within the grid of each of the 2 chambers, ignoring those outside the squares, then multipling the total by 50; this gives the eggs per gram of faeces (e.p.g.). Reading the count should not be delayed beyond the recommended time as the flotation fluid may distort or destroy delicate eggs. Therefore, it is advisable to only process a few samples at a time.
When interpreting McMaster results, it must be remembered that a number of factors can influence the occurrence, recognition or numbers of helminth eggs found in a faecal sample. In particular, the number of eggs is not necessarily indicative of the number of worms present. Reasons for this include: Eggs are produced only by fertile adult female (or hermaphrodite) worms and will, therefore, be absent in immature or single sex infections. The daily output of eggs by fertile females is influenced by host-physiological factors such as stress or lactation (increased) or immunity (decreased). Chemotherapy can also affect egg-production e.g. corticosteroids (increased) or sub-lethal anthelmintic doses (decreased). Some food-stuffs may have a similar effect e.g. tannin-rich forages (decreased). The concentration of eggs (per gram of faeces) is influenced by the daily volume of faeces being produced by the host, the rate of passage by the ingesta through the intestine, and the distribution of eggs throughout the faecal mass. Some types of eggs are heavier than others and may not float well in solutions of lower specific gravity (e.g. Fasciola). Some eggs from different species are indistinguishable (particularly trichostrongylids and strongylids). This complicates clinical interpretation as some species (e.g. Haemonchus) produce many more eggs per day than others (e.g. Ostertagia).
The mean EPG was statistically significant for male and female animals for Eimeria (p=0.017) and Trematodes (p=0.006). Although in this study, mean EPG Eimeria was higher in males (68.6) than females (12.1), and Trematodes male (0.34) and females (0). Female animals are ideally more prone to helminth infections physiologically because of stress, pregnancy and lactation conditions which compromise their immunity. The mean Strongyle EPG was 1056.1 in camels and 323.1 in donkeys. The mean Strongyle EPG between species, camel and donkey was significant at (p=0.020). It could be explained that donkey is a hardier animal, closer to wildlife species. Hence, it has a stronger resistance to infections naturally, more tendency as a reservoir host. However, fewer donkeys than camels were sampled in this study.

Conclusion
Helminthes infection is endemic in camels and donkeys in Uganda. A wide range of species of helminthes that plague donkeys and camels was detected in Karamoja sub-region, Uganda. The observation of multiple infections with high prevalence and high overall EPG suggest the presence of favorable environmental conditions for survival, infection and perpetuation of helminthes of camels and donkeys in Uganda. There is complete lack of veterinary service provision to these animals and lack of awareness of animal welfare. Information on the different aspects of parasitology of these animals is also limited. Production and productivity of camels and donkeys in Uganda is compromised by the little or no veterinary care and welfare of these animals.