Prevalence of gastro-intestinal parasites of donkeys in Dugda Bora District, Ethiopia

 G Ayele, G Feseha, E Bojia and A Joe*

Addis Ababa University, Faculty of veterinary medicine, P.O.Box 1973, Debre Zeit, Ethiopia
^*Donkey sanctuary UK Sidmouth Devon, UK
ayelegizachew@yahoo.co.in

Abstract

A year round study (from October-2004 to September-2005) was conducted in Dugda Bora district (Ethiopia) to identify the gastrointestinal parasites of donkeys, determine their prevalence rates and find associations between measurable parameters and parasites burden.

A total of 339 faecal samples were collected randomly for qualitative and quantitative faecal analysis. The parasites encountered were Strongyle (100%), Parascaris equorum (50%), Anoplocephala Spp. (7.4%), Gastrodiscus aegypticus (6%), Oxuris equi (3%) and Fasciola (1.5%). Gross faecal examinations revealed Gasterophilus intestinalis and Gasterophilus nasalis (20.9%). 81.7% of donkeys sampled were severely infected, 8.3% heavily, 3.8% moderately and 6.2% mildly infected. Mixed infections were detected in 54.8% of the donkeys. Cultural identification of larvae (n=28) demonstrated Strongylus vulgaris (100%), Cyathostomes (100%), Strongylus edentatus (66.6%), Trichostrongylus axei (40%), Strongloides westeri (33.3%), Triodontophorus (50%) and Dictyocaulus arnfieldi (20%). Rainy season encouraged Strongyle infection and there was no significant age associated immunity (p>0.05) to Strongyle and Parascaris equorum infections. The body condition score and packed cell volume were negatively correlated (r= -0.67 & -0.6, respectively) with the total epg count.  The presumptive clinical examination of donkeys (n=1674) showed that Parasitosis (45%), Parasitosis and wounds (16.8%), wounds (16.4%), lameness (6%), respiratory complications (5.4%), septicemia (4.2%), sarciod (3.1%) and eye problems (2%) were the health problems in the area.

Parasitism, wounds and other health problems were identified affecting the health and welfare of donkeys and Government or other development agencies should include donkeys in their priority lists of research and develop sustainable integrated diseases prevention and control programs that are practical in developing communities.

Key words: Donkeys, Ethiopia, gastrointestinal parasites, prevalence

Introduction

Despite the increase in mechanization throughout the world, donkeys are still well deserving of the name 'beasts of burden'. They have a prominent position in the agricultural systems of many developing countries. This is shown by the wide spread use of donkeys in rural and urban areas in Africa (Pearson et al 1999). It is suggested that donkeys can play a great role in the frame works of food security and social equity of high food insecure countries.

Ethiopia has about 7.9 million equines, where 5.2 millions are donkeys (CSA 1995). There is one equine for every four people in the agricultural sector and for every five persons of the total population (Wilson 1991).The Domestic donkey of Ethiopia traces its ancestry to the wild asses found in Egypt, the Sudan, Somalia and Ethiopia, namely Equus asinus africanus and Equus asinus somalicus (Feseha 1991). The low level of development of the road transport network and the rough terrain of the country make the donkey the most valuable, appropriate and affordable pack animals under the small holder farming system of Ethiopia (GebreWold et al 2004). Donkeys appear to be an effective entry point for assisting women not only in domestic responsibilities, but also enabling women to be engaged in income-generating activities which otherwise they may not have had access to (Marshall and Ali 2004). Abayneh et al (2002) has revealed that in areas where draft power is a constraint for crop cultivation a pair of well-conditioned donkeys could be used as an alternative draft power sources for secondary and tertiary land preparations.

Even though donkeys have often been described as sturdy animals, they succumb to a variety of diseases and a number of other conditions. (Svendsen 1997).

The attention given by Governmental and non-Governmental organizations to donkeys has been far below to what it deserves. This might be partly due to the wrong perception that the donkey does not require a lot of care, that when donkeys do get sick they are quick to die, and the donkey's low traditional status (Marshall and Ali 2004). Despite the huge numbers and the increasing importance of donkeys in the Ethiopian economy, knowledge about the health problems affecting their welfare is limited for most parts of the country. Therefore, the objectives of this study were

• to determine spectrum of species and prevalence of major GIT parasites involved in donkeys.
• to determine seasonal distribution of donkeys GIT parasites.
• to find associations between measurable parameters and GIT parasites burden.

Materials and methods

Study area

The study was conducted during the year Oct.2004 - Sept. 2005 in Dugda Bora District of Ethiopia which is located about 134 km South of Addis Ababa. The long rainy season in the area is between June and October, while the long dry season lasts from October to February. The mean minimum and maximum temperatures in the area ranges from14 to 27ºC. The average altitude is 1650m above sea level, with an average rainfall of 716mm.

Study animals and protocol

A total of 339 (186 male and 156 female) donkeyswere randomly selected from 12 peasant associations of Dugda Bora district and subjected to quantitative and qualitative coprological examinations to identify the major GIT parasites involved, to determine their prevalence rates and to find associations between measurable parameters and GIT parasites burden.

The farmers in the selected peasant associations were informed on the importance of the study and to present their donkeys on specific visit dates and places. The age of the selected donkeys was determined by dentition (Crane 1997) and body condition scores were subjectively estimated based on the guides published by Svendsen (Svendsen 1997). Donkeys were grouped in to three age categories. Donkeys under two years of age were classed as young (n=64), those in range of two to ten years were classed as adult (n=182) and those beyond ten years were classed as old (n=93). These age classes were based on age of first work, productive age and the life span of Ethiopian donkeys (Yoseph et al 2001; Svendsen 1997).

Faecal samples were taken directly from the rectum or the ground when the animal was seen defecating with strict sanitation and placed in air and water tight sample vials, and then brought to the laboratory. Gross faecal examinations were done before the samples were subjected to microscopic examinations. Modified McMaster and Baerman techniques and sedimentation and floatation methods were used to identify and count eggs or larvae of parasitic helminthes (Urquhart et al 1996; Soulsby 1982). Faecal cultures were done for samples with total mean egg counts of greater than 10,000. Identification of larvae (L₃) was based on specific morphological traits set by Poynter (1970). Levels of worm infection were extrapolated from infection severity index defined by Soulsby (1982) where horses are said to have mild, moderate, heavy and severe nematode infestation if their fecal egg counts are less than 500, 800-1000, 1100-1500 and more than 1500, respectively.

Packed cell volume was determined following centrifugation in a high-speed micro-haematocrit centrifuge (Hawaksly-England) (Daclie and Lewis1991).

Data Analysis

Descriptive statistics were used to determine the prevalence of endoparasites and percentage of health problems in the area. Association of total eggs per gram with body condition score and packed cell volume was determined by Pearson test  (SAS 1998). One-way ANOVA in a General Linear Model (GLM) (SAS 1998) was used to observe the variations of total epg of parasite species with age, seasons and sex groups. In all the analysis, confidence level was held at 95%. 

Results

Macroscopic fecal examination

Gasetrophilus intestinalis and Gasterophilus nasalis were identified on gross faecal examinations with total prevalence of 20.9% (70/338).

Microscopic fecal examination

All samples examined (n=338) were found positive for helminth eggs. Strongyle (100%), Parascaris equorum (50%), Anoplocephala Spp. (7.4%), Gastrodiscus aegypticus (6%), Oxuris equi (3%) and Fasciola (1.5%) eggs were identified. 81.7% of donkeys sampled were severely infected, 8.3% heavily, 3.8% moderately and 6.2% mildly. The highest faecal worm eggs count was recorded in the long rainy season (20143 epg) and the lowest worm egg count (50epg) was recorded in the long dry season.

The statistical associations of total mean epg of GIT parasites with seasons and age groups are located in Tables 1 and 2, respectively. Body condition score was negatively correlated (r=-0.67) with epg counts. There was no statistically significant difference in level of helminth infection between male and female donkeys (p>0.05).

Differential larval counts

Fecal samples with greater than 10,000 epg (n=28) were subjected to coproculture for the identification of infective nematode larvae. Seven types of helminth parasites larvae were identified (Table 3).

Haematocrite (PCV)

Haematocrite (PCV) was negatively correlated (r= -0.6) with the total epg and the mean was 34± 3.71 (mean ± sd), with a range of 25 to 50%.

The presumptive clinical examination findings of the total donkeys used as sampling frame (n=1674) are located in Table 4..

Discussion

Gasterophilus intestinalis and Gasterophilus nasalis were observed on gross faecal examination of faeces with infection rate of 20.9%. These were also observed on rectal mucosa of donkeys with rectal prolapse. Yilma et al (1990) has reported that rectal prolapse is quite common in donkeys of Ethiopia and associated with infection by Gasterophilus larvae.

The microscopic fecal examination showed that helminthosis was an important health disease in the study area. Mixed infections were detected in 54.8% of the donkeys. Based on the severity index defined by Soulsby (1982), 81.7% of donkeys sampled were severely infected, 8.3% heavily infected, 3.8% moderately infected & 6.2% mildly infected. The maintenance of high infection rate of parasitic helminths in the study area might be associated with lack of any parasitic helminths intervention program and the management system in the area where many equines were allowed to graze together on small plots of land through out the year which facilitates contamination between animals.

The prevalence of Strongyle spp. was 100%. This is in harmony with the work of Yoseph et al (2001), Mulate (2005) and Fikru et al (2005) who have reported 100%, 100% and 98.2% in donkeys of Wonchi, high lands of Wollo province and western highlands of Oromia, respectively. Strongyle infestation was significantly higher (p<0.05) in the rainy season of the year. This was in accord with the work of Yoseph et al (2001), Mulate (2005) and Fikru et al (2005) who indicated that fecal worm egg counts begin to rise to severe levels during the wet season. This could be because of the long pre-patent period of the strongylus spp. which ensures that larvae acquired in one grazing (wet) season, only reach maturity during the next (Urquhart et al 2001). From this seasonal variation of strongyle infestation, treatment schedules that enable the elimination of the parasites at peak infection and prevent re-infection of pastures can be proposed. Troncy (1989) has proposed two treatment schedules per year with broad-spectrum anthelminthics for tropical conditions. A treatment may be given at the end of the rainy season. At this time, the animals are well nourished and may harbor large number parasites without being seriously affected. Eliminating these parasites will improve the adaptation of the animals to the harsh dry season conditions. Another treatment can be given at the end of the dry season. This treatment reduces infestation of pastures at the time of first rains and by residual parasites. Although the young had relative higher mean epg, there was no stastically significant difference (p>0.05) between age groups for the level of strongyle andParascaris equorum infections. This might be the effect of mal-nutrition which reduces the host-parasite response and increased land of cultivation which restricts donkeys on small communal grazing land which allows the animals for continuous larvae exposure.

The prevalence of Parascaris equorum was 50%. This is in agreement with Mulate (2005) who reported 43.8% in south and north Wollo provinces. Yoseph et al (2001) and Fikru et al (2005) have reported 15.7% and 17.3%, respectively. These finding are relatively lower than the present finding. This could be because of the smaller sample size used in their study. Level of Parascaris equorum infestation had no significant difference for the different seasons of the year. This might be due to the high resistance of the eggs of Parascaris equorum to desiccation. Soulsby (1982) has stated that Parascaris equorum eggs are very resistant to adverse conditions, like drying or freezing and the larvae rarely hatch and infection usually takes place through ingestion of the eggs. Heavy infections of Parascaris equorum causes impaction and perforation leading to fatal peritonitis (Urquhart et al 1996).We confronted a case of a 15 years old female donkey that died of this complication.

Oxyuris equi with prevalence rate of 6% was very low compared with the work of Yoseph et al (2001) who reported 32.4%. The low prevalence in this study might be the effect of relative higher temperature in the present study area which desiccates the highly susceptible O. equi eggs.

The prevalence of Anaplocephala species was 7.6% .This low prevalence could be due to the seasonality of Orbited mites vectors (Soulsby 1982). Similar results have been reported in the survey of helminthosis conducted in the central high lands of Ethiopia (Yoseph et al 2001).

Lower prevalence (1.5%) of Fasciola was recorded in the present study compared to other reports in the central highlands of Ethiopia (Yoseph et al 2001, Mulate 2005). This lower prevalence might be due to the differences in ecological conditions for the development of intermediate snails and the parasite. Hammami and Ayadi (1999) have reported that permanent dampness, suitable luminosity, basic pH of soil and water, and temperature contribute to the multiplicity of snails. The infections were recorded in April (from snail infection of Nov. - Dec.) and July (from snail infection of March-April). A study conducted by Hardy et al (2002) in Egypt indicated that donkeys are the potential reservoir of Fasciolosis and they recommended that donkeys should be considered within the preventive and control measures of Zoonotic Fasciolosis.

Cultural identification of larvae indicated 100% prevalence of Strongylus vulgaris and Cyathostomes. This is in agreement with the study of Yoseph et al (2001). S. vulgaris is the most pathogenic in Equines, causing unthriftiness, weakness, and increased susceptibility to other infection and even death and fatal colic could also have arisen from strongylid overload (Khallaayoune 1991). Dictyocaulus arnfieldi was recovered in 32% of the fecal cultures. Donkeys act as reservoir of Dictyocaulus arnfieldi and as a source of infection for horses (Beelitz et al1996).

The body condition score was negatively correlated (r= -0.67) with the total mean epg which implies that the body condition score is a good indicator of parasitic burden, which can be used by the resource limited communities to identify donkeys with immediate requirement of anthelmintic remedies.

The mean value of the haematocrit reading was slightly lower than that reported by Saul et al (1997). The variation in haematocrit may be due in part to the low altitude of Dugda Bora District. This variation could also be due to differences in parasitic burden (Egbe-nwiyi and Gana 2003). The packed cell volume was negatively correlated (r=-0.6) with total EPG. Egbe-nwiyi and Gana (2003) have reported that helminthosis in donkeys causes normocytic and normochromic anemia. This result might pave the way for the development of the FAMACHA© system for donkeys where eye color chart can be used as a diagnostic tool for heavy parasitic infections. The use of FAMACHA© system and employment of available potent anthelminitic remedies by poor farmers to treat animals identified with heavy infection appear sustainable and effective approaches to combat worm infection and maintain acceptable levels of goat production in poor farming regions of South Africa (Vatta et al 2003).

A large proportion of donkeys suffered various degrees of wounds. Pearson et al (2003) reported that the main sources of wounds were inappropriate harness, hobbles and saddle design, hyena bite, donkey bite, and car accident, injury by the owners or other people. Harness related problems were raised from incorrect size, inappropriate fitness, too narrow or too thin, made of unsuitable synthetic materials. Poor padding, poor design and synthetic rope to fix the load were the problems related with using pack saddles. Personal observations of the authors and history gathered from the donkey owners confirmed this report.

Cases of Strangles were diagnosed in two young donkeys with signs of persistent bilateral nasal discharge, bilateral swellings in the regions of Viborg's triangle, enlarged retropharyngeal lymphnodes and increased temperature (Rose and Hodgson 2000). Other respiratory complications were increased respiratory rate, dyspnoea, mucoprulent nasal discharge, and coughing that might be symptoms of Bacterial pneumonia, pleuroneumionia, verminous pneumonia and chronic obstructive pulmonary disease (COPD) (Rose and Hodgson 2000).

Thrush, cracked heel, hoof abscess, hoof keratoma and hoof overgrowth were the hoof abnormalities confronted. Nails, thorns, and other sharp objects were removed from the sole-wall junction or white line of abscessed hooves. There is no regular hoof care of working donkeys in the area which exacerbated the problems. Feseha (1997) has reported that the predisposing factors for hoof problems of Ethiopian donkeys are related with poor hoof care and poorly drained yards where donkeys stand for lengthy period in mud. A case of mild tetanus was handled. This donkey had abscessed hoof which might be the route of entry and proliferation of clostridium tetani organisms (Blood et al 1983).

Sarcoids were observed in 3.1% of donkeys. Yilma et al (1990) has indicated that sarcoids are a common skin tumour in donkeys of central highlands of Ethiopia. The clinical appearances of sarcoids were fibroblastic, verucose, nodular and mixed types (Pascoe and Knottenbelt 1999).

Conclusions

• Helminthosis, wounds and other health problems were identified affecting the health and welfare of donkeys in the study area.

• Government or non profitable development agencies should include donkeys in their priority lists of research and develop sustainable integrated diseases prevention and control programs that are practical for developing communities.

Acknowledgment

We are grateful to the Donkey health and welfare project in Ethiopia for the supply of all study materials. We are also grateful to the Veterinary department staff and donkey owners of Dugda Bora district for their support and cooperation in the study period.

References

Abayneh T, Gebreab F, Zekarias B and Tadesse G 2002 The potential role of donkeys in land tillage in central Ethiopia. Bulletin of Animal Health and Production in Africa. 50, 172-178.

Beelitz P, Gobel E and Gothe R 1996 Endoparasites of donkeys and horses kept in communal housing in Upper Bavaria; species spectrum and incidence. Tierarztl prax.24(5): 471-5.

Blood D C, Rodostits O M and Henderson J A 1983 Diseases caused by Clostridium spp. In: Veterinary Medicine, a textbook of the diseases of Cattle, Sheep, Pigs, Goats and Horses, 6^th edition.Bailliere Tindall, 1^st Annes Road, East bourne, East Sussex BN21. Pp. 536-539.

Crane M 1997 .Medical. In: The professional hand book of the donkey, 3^rd edition. Pp.19-36, Whittet Books Limited, 18 Anley Road, London W14 OBY.

CSA 1995 Central Statistical Authority of Ethiopia. Agricultural samples survey volume II. Statistical Bulletin 132, Addis Ababa.

Daclie S J V and Lewis S M 1991 Determination of packed cell volume. In: Practical Haematology. Churchill Livingstone, Medical Division of Longman Group UK limited., 48-51.

Egbe-nwiyi T N and Gana S M 2003 Gastro-intestinal Helminths of Donkeys in Maiduguri: The Heamatological changes. Tropical Veterinarian 21(1), 53-57.

Feseha G 1991 Use of equines in Ethiopia. In: proceedings of fourth livestock improvement conference. Pp. 51-58, Institute of agricultural research, Addis Ababa, Ethiopia.

Feseha G 1997 Diseases and Health Problems of the Donkey Abroad. In: The professional hand book of the donkey, 3^rd edition. Pp.207-226, Whittet Books Limited, 18 Anley Road, London W14 OBY.

Fikru R, Reta D and Bizunesh M 2005 Prevalence of equine gastrointestinal parasites in western high lands of Oromia, Ethiopia. Bulletin of Animal Health and Production in Africa. Pp. 161-166.

Gebre Wold A, Tegegn A and Yami A 2004 Research needs of donkey utilization in Ethiopia. In: Fielding and Starkey P (editors). Donkeys, People and Development. A resource book of the animal traction network for eastern and Southern Africa (ATNESA), Technical center for agriculture and rural cooperation (CTA), Wageningen, The Netherlands, pp. 77-81, ISBN 92-9081-219-2.

Hammami H and Ayadi A 1999 Ecology of Lymnaea truncatula Muller, intermediate host of Fasciola hepatica Linne in the microclimate of Tozeur (southeast of Tunisia). Bulletin de la Société de Pathologie Exotique 92 (5):302-4.

Hardy F M, Morsy T A, Gawish N I, Antonios T N and Abdel Gaward A G 2002 The potential reservoir role of donkeys and horses in zoonotic fasciolosis in Gharbia Governorate, Egypt. Egyptian Society of Parasitology, 32 (2):561-70.

Khallaayoune K 1991 Benefit of a strategic deworming program in working donkeys in Morocco. In: Fielding D and Pearson RA (editors) Donkeys mules and horses in Tropical Agricultural Development. Pp.174-180, CTVM Edinburgh.

Marshall K and Ali Z 2004 In: Fielding and Starkey P (editors). Donkeys, People and Development. A resource book of the animal traction network for eastern and Southern Africa (ATNESA). Technical center for agriculture and rural cooperation (CTA), pp. 77-81, Wageningen, The Netherlands,. ISBN 92-9081-219-2.

Mulate B 2005 Preliminary study on helminthosis of Equines in south and north Wollo Zones. Journal of Veterinary Association. 9(2): 25-37.

Pascoe R R R and Knottenbelt D C 1999 Equine Sarcoid. In: Manual of Equine Dermatology. W B Saunders, Harcourt Publishes Limited, 24-28Oval Road, NW1 7DX, UK.Pp. 244-52.

Pearson R A, Nengomasha E and Krecek R C 1999 The challenges in using donkeys for work in Africa. In: Starkey PH, Kaumbutho P (editors). Meeting the Challenges of Animal Traction . A resource book of the Animal Traction Network for Eastern and Southern Africa (ATNESA), pp. 190-198, Harare, Zimbabwe. Intermediate Technology Publications, London.

Pearson R A, Simalenga T E and Krecek R 2003 Harnessing and Hitching donkeys, horses and mules for work. 34p. University of Edunburgh, Center for Tropical Veterinary Medicine, Eastern Bush, Roslin, Midlothianm, EH25 9 RG, Scotland.

Poynter D 1970 Some observations on the nematode parasites of horses. In: Bryans J T, Gerber H (editors), Equine Infectious Diseases. Proceedings 2nd International Conference on Equine Infectious Diseases, Paris, (Basel, Switzerland, S.Karger), Pp. 269-289.

Rose R F and Hodgson D R 2000 Manual of equine practice.2^nd edition. 818p, Philadelphia, W B Saunders Company.

Saul C, Siefert L and Opuda-Asibo J 1997 Disease and Health problems of donkeys: a case study from eastern Uganda. In: Improving donkey utilization and management. ATNESA workshop, 5-9, Debre Zeit, Ethiopia. Pp58-63.

Soulsby E 1982 Helminths, Arthropds and Protozoa of Domestic Animals. 7^th edition, 790p. Balliere Tindall, 1^st Annes Road, East bourne, East Sussex BN21.

Svendsen E D 1997 Parasites abroad. The professional hand book of the donkey, 3^rd edition. Pp.166-182, Whittet Books Limited, 18 Anley Road, London W14 OBY, Pp.166-182.

Troncy P M 1989. Helminths of Livestock and Poultry in Tropical Africa. In: Manual of Tropica Veterinary Parasitology. The Technical center for Agricultural and Rural Co-operation (CTA).PP. 1-178, CAB International, Walling ford, Oxon OX10 8DE, UK.

Urquhart G M, Armour J, Duncan J L, Dunn A M and Jennings F W 1996 Veterinary Parasitology.2nd ed.307p. Black well Science limited, London.

Vatta A F, Letty B A, Van der Linde M J, Van Wijk E F, Hansen J W and Krecek R C 2001. Testing for clinical anaemia caused by Haemonchus spp. in goats farmed under resource-poor conditions in South Africa using an eye colour chart developed for sheep. Veterinary Parasitology. 2001 99:1-14.

Wilson R T 1991 Equines in Ethiopia. In: Fielding , Pearson R A (editors). Donkeys Mules and horses in tropical agricultural development. Edinburgh, Scotland. Pp. 33-47, Center for tropical Veterinary Medicine, University of Edinburgh.

Yilma J, Svendsen E and Mohamed A 1990. Health problems of working donkeys in Debre Zeit and Menagesha of Ethiopia. In: Fielding D and Pearson R A (editors). Donkeys, Mules and Horses in Tropical Development. Proceedings of a colloquium Held in Edinburgh, Scotland, (Edinburgh, University of Edinburgh), Pp. 151-166.

Yoseph S, Feseha G and Abebe W 2001. Survey on helminthosis of equines in Wonchi, Ethiopia. Journal of the Ethiopian Veterinary Association 2001, 5, 47-61.

Received 11 July 2006; Accepted 23 September 2006; Published 27 September 2006

Go to top