Yoseph Shiferaw
1
Seasonal variation in the parasite burden and body condition of
2
working donkeys in East Shewa and West Shewa regions of Ethiopia
3
4
Yoseph S.1, Smith D.G.2, Mengistu A.1, Teklu F.3, Firew T.1 and
5
Betere Y.1
6
7
1
8
2003, Addis Ababa, Ethiopia. E-mail iar@telecom.net.et
Ethiopian Agricultural Research Organisation, Holetta Research Centre, PO Box
9
10
2
11
Scotland, UK, AB24 3FX. Email d.g.smith@abdn.ed.ac.uk*
Department of Agriculture and Forestry, University of Aberdeen, Aberdeen,
12
13
3
Oromia Agricultural Research Institute, Adami Tulu, PO Box 35, Zway, Ethiopia.
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15
*Address to which correspondence should be sent
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17
Keywords
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Helminths, Donkey, Ethiopia,
19
1
Yoseph Shiferaw
2
1
Abstract
2
A yearlong survey of donkeys arriving at markets in three localities in East and West
3
Shewa regions of central Ethiopia was carried out during 2002. Total faecal worm
4
egg counts and body condition scores were measured for a total of 963 donkeys over a
5
twelve-month period.
6
between localities but there was significant (p<0.001) seasonal variation within
7
localities.
8
lowest (956 eggs per gram of faeces) at the end of the long dry season (February) and
9
highest (2022 eggs per gram of faeces) in the middle of the long wet season (August).
10
Body condition score was closely associated with level of helminth infection
11
(Goodman-Kruskal measure of association 0.60 - 0.80). Seasonal variation in body
12
condition score reflected the temporal changes in worm burden and the availability of
13
forage. It is suggested that a body condition score of three or less could be used as a
14
simple means of identifying donkeys that require therapeutic treatment with
15
anthelmintic. Its is further proposed that economically viable, strategic control of
16
helminths could be achieved by administrating donkeys with a single annual dose of
17
avermectin based anthelmintic at the start of the long rainy season (May - June). This
18
may allow donkeys to recover body condition when available forage was most
19
abundant and nutritious.
20
supplementation is provided during the later part of the dry season (November -
21
January) this may help maintain body condition when forage is scarce and the
22
helminth challenge is at its lowest.
23
Total faecal worm egg counts did not differ significantly
Levels of helminth infection closely followed rainfall patterns, being
It is also recommended that protein rich feed
Yoseph Shiferaw
3
1
Introduction
2
Throughout Ethiopia donkeys are used to transport goods between homestead, field
3
and market (Feseha et al. 1997). In remote rural areas of the country where modern
4
transportation is not available the contribution of donkeys in facilitating marketing of
5
agricultural products is of paramount importance (Pearson 2000). Donkeys have
6
reduced the domestic transport burden of rural people especially women and have
7
created employment and income generating opportunities for many people (Pearson
8
2000). Studies have shown that transport constitutes one of the necessary inputs for
9
rural development and has a positive stimulus for growth in food production, poverty
10
alleviation and overall communication (Pearson 2000).
11
Although donkeys are often described as hardy and resistant animals, they do
12
succumb to a number of health problems. The most important ones are parasitic
13
diseases especially gastrointestinal parasites, harness sores, sarcoids and infectious
14
diseases such as anthrax.
15
problem of donkeys in Africa, contributing to poor body condition, reduced power
16
output, poor reproductive performance and short lifespan. Large number of internal
17
parasites has been reported in a study of five African countries including Ethiopia,
18
Kenya, Zimbabwe, Burkina Faso, Chad and Morocco (Pandey et al., 1994).
19
In Ethiopia various studies have shown that donkeys commonly harbour
20
gastrointestinal parasites such as large and small strongyle, ascarids, pinworms, bots,
21
stomach worms, lungworms, tapeworms and live flukes (Yilma et al., 1991; Feseha et
22
al., 1991; Pandey et al., 1994; Yoseph et al., 2001). Despite these comprehensive
23
surveys of the prevalence and distribution of different helminth species little
24
information is available on the seasonal dynamism of helminthiasis and the effect of
25
parasitism on body condition and work performance of donkeys.
Gastrointestinal parasites are the most serious health
Yoseph Shiferaw
4
1
The aim of this study is study the seasonal variation of helminthiasis, body condition
2
and work performance of donkeys in three areas of Ethiopia. This information will be
3
used to support the development of helminth control strategies that can help donkey
4
owners limit the parasite burden of their animals as cost effectively as possible.
5
6
Materials and Methods
7
The study was conducted in three agro-ecological zones of East and West Shewa
8
regions of Ethiopia during 2002. The surveys were carried out at peri-urban market
9
places close to research stations at Holetta (high altitude), Debre Zeit (mid-altitude)
10
and Adami Tulu (low altitude). Detailed descriptions of the farming systems, climate
11
and topology of the three zones were published by Mengistu et al. 2005.
12
The study was conducted on faecal samples collected from every tenth donkey
13
arriving at three market areas within each zone.
14
sampled, 298, 376 and 289 from Holetta, Debre Zeit and Adami Tulu respectively.
15
The age (determined by dentition) and sex of each donkey were recorded. Animals
16
were grouped into two age categories, donkeys under two years of age were classes as
17
young and donkeys older than two years of age classed as adult.
18
Body condition scores were estimated using the guide published by Pearson and
19
Ouassat (2000).
20
assess and record the physical condition and health of the animals.
21
After assessing the physical condition of each donkey faecal samples were collected
22
directly from the rectum. On-the-spot gross examination of faecal samples were made
23
to look for evidence of parasites such as Anoplocephala spp, Trichonema spp,
24
Gastrophilus spp and Oxyuris equi. Specimens were put in plastic bottle labelled with
25
identification number and placed in icebox for later laboratory examination.
A total of 963 donkeys were
Each donkey was visually examined by a veterinarian in order to
Yoseph Shiferaw
5
1
Quantitative and qualitative faecal helminth egg examinations were done employing
2
modified Mc-Master method (Kassai, 1999). Modified Baermann technique was used
3
to ascertain the occurrence of lungworm infection in a fresh sample (Sloss et al.,
4
1994). In addition ova culture were made in wet season for specific identification and
5
quantification of GIT helminths. Identification of larvae (L3) was based on specific
6
morphological traits set by Poynter (1970).
7
The study was supported by standard and through post-mortem examination of two
8
young and two adult donkeys from high land and low land areas. Post-mortem worm
9
examination was conducted in accordance with standard procedures and techniques
10
(Hansen and Perry, 1994). The contents of each parts of the gut was separately
11
opened in to a container and irrigated by water followed by parasitological
12
examination (collection, identification and counting).
13
Collected data were analysed using Minitab Release 14.12.0.
14
intensity and distribution of helminth infection group means were used after logarithm
15
transformation of the original data set in order to reduce skewedness. One-way
16
ANOVA was carried out on data from each location in order to determine statistical
17
differences between survey months. Associations between body condition score and
18
level of infection were measured with Ordinal Logistic Regression using Minitab
19
Release 14.12.0.
To estimate the
20
21
Results
22
The numbers of male, female, a young and adult donkey sampled from each location
23
during the survey is shown in table 1.
24
In all the study areas the highest faecal worm egg count was recorded in the long
25
rainy season of the year (June – October) and the lowest worm egg count was
Yoseph Shiferaw
6
1
recorded in the long dry season (October – February) (Figure 1 and 2). The seasonal
2
trends of faecal worm egg count were statistically similar in all the study locations
3
(Figure 2). However, there were highly significant differences (p < 0.001) in faecal
4
worm egg counts between months in each study location. Data were not collected in
5
Adami Tulu during February due to logistic difficulties.
6
Levels of worm infection in donkeys were determined from total faecal egg count of
7
donkeys from the three study locations. Using the infection severity index defined by
8
Soulsby (1982) for horses (where an average total faecal nematode egg count of less
9
than 500 eggs per gram (epg) suggests a mild infection, 800–1000 a moderate
10
infection, 1100 – 1500 a heavy infection and more than 1500 a severe infection), the
11
mean level of infection in the donkeys in all study locations did not fall below
12
moderate in any month (Figure 2). In all locations monthly faecal worm egg counts
13
closely followed rain patterns (Figure 1 and 2).
14
Monthly variation in infection was least at Adami Tulu (range in faecal egg count 923
15
–1901 epg) and greatest at Holetta (range in faecal egg count 1005 – 2072 epg). At
16
Holetta levels of infection remained at moderate levels from December until March,
17
rising to severe levels by June through until September. At Debre Zeit levels of
18
infection remained at moderate levels from November until May, rising to severe
19
levels only between July and September. At Adami Tulu levels of infection were
20
moderate in October and remained at moderate levels between February until April,
21
rising to severe levels between July and September.
22
Young donkeys (<2years old) had significantly higher faecal worm egg counts
23
compared to adult donkeys from the same location (Table 2).
24
statistically significant difference in level of infection between male and female
25
donkeys from the same location.
There was no
Yoseph Shiferaw
7
1
There was a significant (p<0.01) association between body condition score of donkeys
2
in each study area and level of gastrointestinal parasitic infections. Goodman-Kruskal
3
measure of association (Kianifard and Chen, 1999) was 0.62, 0.80 and 0.60 in Holetta,
4
Debre Zeit and Adami Tulu respectively. Donkeys with body condition score of four
5
or above had significantly (p<0.001) lower levels on infection compared to donkeys
6
with body condition scores of three or less (Figure 3).
7
In all three localities the number of animals with a body condition score of 3 or less
8
tended to increase progressively over the course of the long dry season from October
9
to January, despite diminishing levels of infection during this period (Table 3). This
10
probably reflects the diminishing availability of forage during this period.
11
Qualitative faecal egg analysis was only conducted at Holetta and Debre Zeit to
12
differentiate the types of parasites and their relative occurrence. Six types of eggs
13
were identified namely Strongyle spp., Dictyocaulus arnifieldi, Parascaris equorum,
14
Anoplocephala spp, Gastrodiscus aegypticus and Oxyuris equi. Donkeys sampled
15
were 100% positive for strongyle egg in both study areas. A relatively low number of
16
Parascaris equorum were identified probably due to mature age of donkeys sampled
17
from the market.
18
The study was supported by post-mortem examination of two young and two adult
19
donkeys from Holetta and Debre Zeit land and low land areas. In general 15 species
20
of gastrointestinal parasites were identified. The identified species were
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Trichostrongylus axei, Habronema musca, Gastrophilus nasalis, Gastrophilus
22
intestinalis, Anoplocephala spp, Parascaris equorum, Strongylus vulgaris, Strongylus
23
edentatus, Strongylus equinus, Triodontophorus spp, Oesophagodontus spp,
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Gyalocephlus capitatus, Cyathostomes, Fasciola hepatica and Fasciola gigantica.
Yoseph Shiferaw
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1
The presence of those parasites was associated with visible gross pathological
2
changes. In the lung, fluid filled hydatid cyst, were found. In stomach there were
3
nodules on the gastric mucus, catarrhal gastritis, and large number of t. axei attached
4
to the mucus membrane. In cardiac and fundus area there was ring like thickening
5
around the attachment of Gastrophilus spp. In small intestine at sites of
6
Anoplocephala spp attachment there was inflammation and thickening. There were
7
also nodules of different sizes with purulent content and small larva in it. In large
8
intestine, small and large strongyles were found in massive numbers attached to the
9
mucus membrane of caecum and colon.
10
There was mechanical damage of liver parenchyma with interstitial hepatitis probably
11
induced by migrating larvae. The bile ducts were extensively filled with a number of
12
adult fluke. Migrating larvae of large strongyles had caused arteritis and in the main
13
branch of cranial mesenteric artery there was inflammation of the wall, thickening and
14
dilation of the wall of the arteries, purulent yellowish nodules.
15
Discussion
16
Quantitative faecal analysis showed the existence of high degree of infection of
17
donkeys by helminth parasites throughout the year. This finding is in agreement with
18
other studies (Yilma et al., 1991; Feseha et al., 1991 and Yoseph et al., 2001). In all
19
three of the study locations level of helminth infection showed significant seasonal
20
variation, these fluctuations were closely related to rainfall patterns across the year.
21
During periods of the year when rainfall are low helminth infections levels fell to
22
moderate levels, giving donkeys some respite from the deleterious effects of severe
23
worm burdens (Figures 1 and 2). Unfortunately, most of these periods of lowest
24
worm burden coincide with periods of the year when the nutritional status of donkeys
25
does not allow recovery of body condition (Table 3).
Yoseph Shiferaw
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1
Body condition score was closely associated with the level of helminth infection. The
2
greater part of the variation in body condition score (60 – 80%) was explained by the
3
variation in faecal worm egg count. This implies that body condition score could be
4
used as a reliable indicator of parasite burden, which could be used by owners to
5
identify donkeys with an acute therapeutic requirement for anthelmintic.
6
Mengistu et al. 2005 showed that donkeys with moderate helminth infections in the
7
same localities as the present study, were able to maintain normal blood parameters
8
and statistically similar weight gains to donkeys that had received intensive
9
anthelmintic treatment or feed supplementation; significantly better weight gains were
10
only achieved when anthelmintic and feed supplementation were combined.
11
Combining anthelmintic treatment with feed supplementation is probably beyond the
12
means of most donkey owners in Ethiopia (Agajie et al. 2000).
13
Furthermore, intensive use of anthelmintic increases the risk of development of
14
resistant strains of helminths (Coop and Kyriazakis, 2001) and some anthelmintics
15
(avermectins) are potentially damaging to the environment (Edwards et al. 2001).
16
Therefore, minimising anthelmintic use to control worm burdens makes economic,
17
therapeutic and ecological sense.
18
Matthee et al.(2002) have shown that a single treatment of moxidectin anthelmintic
19
reduced faecal worm egg counts for up to eight months in working donkeys in South
20
Africa. Similar long-term effects of anthelmintics were demonstrated by Mengistu et
21
al. (2005) in Ethiopian donkeys. The present study has indicated that faecal worm
22
egg counts begin to rise to severe levels during June after the long rainy season begins
23
in May. If donkeys were routinely dosed with avermectin anthelmintic at the end of
24
May or the beginning of June, parasite burdens would be reduced to mild levels for a
25
period of at least four months until the end of the rains in September. This period of
Moreover,
Yoseph Shiferaw
10
1
time coincides with the season when forage is most abundant and of highest quality.
2
Relatively low worm burdens at this time would give donkeys the opportunity to
3
recover body condition before the long dry season.
4
Supplementary feeding of donkeys with a high protein supplement during November
5
through to January when forage was in short supply would help to maintain both body
6
condition and resistance to worm reinfection (Coop and Holmes, 1996). Animals that
7
fall below a body condition score of four during this period could be given a
8
therapeutic dose of anthelmintic.
9
The present study has provided information that may facilitate the development of
10
both therapeutic and strategic worm control. Body condition score appears to be a
11
useful indicator of worm burden and could be used as a guide to identify donkeys that
12
require therapeutic dosing of anthelmintic. Seasonal variation in helminth burdens
13
may provide a window of opportunity when a single strategic dose of avermectin
14
anthelmintic at the start of the long rains can allowed recovery of body condition
15
when feed is abundant. Supplementary feeding (backed up with therapeutic dosing of
16
anthelmintic for donkeys with a body condition score of less than four) could help to
17
maintain body condition when helminth challenge are at their lowest.
18
research is required to test these proposed strategies.
Further
19
20
Acknowledgement
21
The financial support of the Department for International Development (DFID) is
22
gratefully acknowledged. The Ethiopian Agricultural Research Organization is also
23
gratefully acknowledged for facilitating the project. Our sincere gratitude goes to the
24
Holetta, Debre Zeit and Adami Tulu Research Centres for hosting and resource
25
allocation during the project. Special thanks are due to Drs Zinash Sileshi and Anne
Yoseph Shiferaw
11
1
Pearson for their support from the time of planning to implementation. Above all, our
2
appreciation goes to the farmers willing to participate in the project.
3
4
References
5
Agajie, T., Tamirat, D., Pearson, R.A. and Temesgen, T., 2000. Socio-economic
6
circumstances of donkey use and management in the rural and urban areas of central
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parts of Ethiopia. In: D.G. Smith, T. Agajie and L. More (eds), Alleviating Poverty in
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Peri-Urban Ethiopia by Improving the Health, Welfare and Management of Donkeys.
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Promoting Peri-Urban Livelihoods Through Better Donkey Welfare. Proceedings of a
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Workshop Held at Debre Zeit, Ethiopia, October 2000 (Edinburgh, CTVM), 16-18
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Coop, R.L. and Kyriazakis, I., 2001. Influence of host nutrition on the development
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and consequences of nematode parasitism in ruminants. Trends in Parasitology 17,
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325-330
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Coop, R.L. and Holmes, P.H., 1996. Nutrition and parasite interaction. International
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Journal for Parasitology 26, 951-962
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Edwards, C.A., Atiyeh, R.M. and Rombke, J., 2001. Environment impact of
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avermectins. Reviews of Environmental Contamination and Toxicology 171, -137
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Feseha, G., Alemu, G., Friew, K., Abule, I. and Yilma, K., 1997. Donkey utilisation
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and management in Ethiopia. In: P. Starkey and D. Fielding (eds), Donkeys, People
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and Development. Animal Traction Network for Eastern and Southern Africa
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Workshop 5-9 May 1997, Debre Zeit, Ethiopia ATNESA), 46-52
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Feseha, G., Mohamed. A and Yilma, J., 1991. Vermicular endoparasitism in donkeys
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of Debre-Zeit and Menagesha, Ethiopia: Strategic Treatment with Ivermectin and
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Fenbendazole. In: D. Fielding and R.A. Pearson (eds), Donkeys, Mules and Horses in
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Tropical Development. Proceedings of a Colloquium Held in Edinburgh, Scotland,
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3rd - 6th September, 1990 (Edinburgh, University of Edinburgh), 156-166
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Hansen, J. and Perry, B.D. 1994. The Epidemiology, Diagnosis, and Control of
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Helminth Parasites of Ruminants: a Handbook. 2nd edn, Nairobi, Kenya:
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International Laboratory for Research on Animal Diseases.
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Kassai, T. 1998. Veterinary Helminthology. Oxford: Butterworth-Heinemann.
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Kianifard, F and Chen, M., 1999. Extending Goodman-Kruskal's Gamma to the
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Comparison of ordered treatments in multicentre clinical trials. Journal of
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biopharmaceutical statistics 9, 521-529
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Matthee, S., Krecek, R.C., Milne, S.A., Boshoff, M. and Guthrie, A.J., 2002. Impact
12
of management interventions on helminth levels, and body and blood measurements
13
in working donkeys in South Africa. Veterinary Parasitology 107, 103-113
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Mengistu, A., Smith, D.G., Yoesph, S., Nega, T., Zewdie, W., Kassahun, W., Taye, B.
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and Firew, T., 2005. The effect of providing feed supplementation and anthelmintic to
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donkeys during late pregnancy and lactation on live weight and survival of dams and
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their foals in central Ethiopia. Tropical Animal Health and Production in press,
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Pandey, V.S., Khallaayoune, K., Ouhelli, H. and Dakask, A., 1994. Parasites of
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donkeys in Africa. In: M. Bakkoury and R. Prentis (eds), Working Equines:
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Proceedings of the Second International Colloquium on Working Equines, Morocco,
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19 to 22 April 1994 (Rabat, Morocco, Institut Agronomique et Vétérinaire Hassan II.),
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35-44
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Pearson, R.A. and Ouassat, M. 2000. A Guide to Live Weight Estimation and Body
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Condition Scoring of Donkeys. Edinburgh: Centre for Tropical Veterinary Medicine,
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University of Edinburgh.
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Pearson, R.A., 2000. Introduction to the project 'Use and management of donkeys by
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poor societies in peri-urban areas in Ethiopia'. In: D.G. Smith, T. Agajie and L. More
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(eds), Alleviating Poverty in Peri-Urban Ethiopia by Improving the Health, Welfare
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and Management of Donkeys. Promoting Peri-Urban Livelihoods Through Better
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Donkey Welfare. Proceedings of a Workshop Held at Debre Zeit, Ethiopia, October
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2000 (Edinburgh, CTVM)-35
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Poynter, D., 1970. Some observations on the nematode parasites of horses. In: J.T.
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Bryans and H. Gerber (eds), Equine Infectious Diseases. Proceedings 2nd
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International Conference on Equine Infectious Diseases, Paris, 1969. (Basel,
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Switzerland, S. Karger), 269-289
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Sloss, M., Kemp, R. and Zajac, A. 1994. Veterinary Clinical Parasitology. 6th edn,
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(Ames, Iowa State University Press)
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Soulsby, E. 1982. Helminths, Arthropods and Protozoa of Domestic Animals. 7th edn,
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(London, Balliere Tindall)
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Yilma, J., Feseha, G., Svendsen, E. and Mohamed, A., 1991. Health problems of
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working donkeys in Debre Zeit and Menagesha of Ethiopia. In: D. Fielding and R.A.
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University of Edinburgh), 151-166
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2
Wonchi, Ethiopia. Journal of the Ethiopian Veterinary Association 5, 47-61
3
14
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1
Table 1: Total number of donkeys sampled during the survey from each study area
2
categorised by age and sex
Study area
Number of
Age
Sex
Donkeys
Adult
Young
Male
Female
Holetta
298
258
40
183
115
Debre Zeit
376
329
47
251
125
Adami Tulu
289
277
12
175
114
Total
963
864
99
609
354
3
4
5
Table 2:
6
in each study area.
Study area
Holetta
Mean total faecal worm egg counts outputs of young and adult donkeys
Age
n
Mean faecal worm egg counts (epg)
Young
40
1556 ( 0.5)
Adult
258
1285 ( 0.6)
Young
47
1678 ( 0.7)
Adult
329
1140 ( 0.6)
Young
12
1965 ( 0.7)
Adult
277
1217 ( 0.6)
Significance
p < 0.05
Debre Zeit
p < 0.001
Adami Tulu
7
8
p < 0.01
Yoseph Shiferaw
1
Table 3.
2
16
The percentage of donkeys (%) in each month of the survey with body
condition score of between two to six in the three study areas.
Body Condition Score
Study area
Holetta
Debre Zeit
Adami Tulu
3
4
Month
January
February
March
April
May
June
July
August
September
October
November
December
Mean
January
February
March
April
May
June
July
August
September
October
November
December
Mean
January
March
April
May
June
July
August
September
October
November
December
Mean
2
16
13
17
17
5
9
20
0
4
4
0
16
11
4
0
3
3
5
19
4
12
0
10
4
13
6
10
6
0
0
4
0
5
0
3
10
7
4
3
63
39
48
31
35
50
40
59
48
44
33
47
41
41
30
39
43
45
63
54
60
50
31
33
38
44
56
59
38
46
46
50
55
42
43
44
65
56
4
13
35
22
41
45
35
32
36
35
36
40
26
34
41
48
45
37
42
13
29
24
40
36
26
33
35
19
29
38
39
25
17
20
29
27
27
14
26
5
0
6
4
7
15
3
8
5
9
16
27
11
10
11
12
9
9
3
6
14
0
5
21
26
10
11
14
0
24
11
18
21
15
21
17
10
10
15
6
9
6
9
3
0
3
0
0
4
0
0
0
4
4
9
3
9
5
0
0
4
5
3
11
5
5
5
6
0
4
7
10
5
4
10
10
3
6
n
32
31
23
29
20
34
25
22
23
25
15
19
27
33
33
35
38
32
28
25
20
39
27
39
21
17
29
28
28
29
20
28
30
30
29
Yoseph Shiferaw
1
Figure 1.
2
17
Monthly rainfall (mm) measured at the three study locations during
2002.
3
4
Figure 2.
5
Monthly mean total worm egg counts ( s.e.) of donkeys sampled in
the three survey locations.
6
7
8
Figure 3.
The mean total worm egg counts ( s.e.) of donkeys of different body
condition scores in the three study locations.