prevalence of blood and internal … of blood and internal parasites in sheep to be slaughtered in...
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PREVALENCE OF BLOOD AND INTERNAL PARASITES IN
SHEEP TO BE SLAUGHTERED IN KHARTOUM STATE
Sudan
By
ABDELBASIT AHMED EDREES MOHEMED
(B. V. M. 2003, University of Khartoum)
Supervisor
DR. KHITMA HASSAN ELMALIK
(B. V. Sc., M. V. Sc., Ph. D.)
A Thesis Submitted to the University of Khartoum in Partial
Fulfillment of the Degree of Master of Tropical Animal Health,
(M. T. A. H.)
Department of Preventive Medicine and Veterinary Public Health,
Faculty of Veterinary Medicine, University of Khartoum
December 2006
I
To:
My parents and my sister
Soul of my grand mother
Soul of my grand father
My brothers... and my friends...
II
AKNOWLEDGEMENT
Thanks first and last to Allah, who gave me the health, strength and
makes this work possible. My appreciations and best thanks to:
• Dr. Khitma Hassan El Malik for her keen supervision and
valuable guidance.
• Dr. Atif Al Amin A. Gadir for data analysis and unlimited
help.
• The staff of the Department of Preventive Medicine and
Veterinary Public Health, especially Mr. Ahmed A. Wahid
for technical help and Mr. Babo Mahmoud for his efforts
during samples collection.
• My colleagues, especially Dr. Hatim A. Altahir for
providing transport during different stages of the study, also
my best thanks for Dr. Mohammed A.Elmoneim, Dr.
Mohammed Siddig Al Arabi, Dr. Mohammed El Wasik and
Dr. Ibrahim M. Elhassan for helping me in samples
collection.
• My brother Abd-El Elah Ahmed for the unlimited help and
continuous support.
VII
Abstract
This study was conducted on sheep brought from different states
of Sudan (Kordofan, White Nile, Darfour and Algadarif) to Khartoum
State to be slaughtered for local consumption and export. The study
conducted in three slaughter houses in the three towns of the state in the
period between April to June 2006, to investigate the prevalence of blood
and internal parasites and to assess the relationship between the
occurrence of these parasites and factors of, body temperature, origin,
breed, age and sex. A total of 150 samples were examined during this
study.
The results showed that, the prevalence of blood parasites was 15.3%,
Theileria spp. showed the highest prevalence rate (14.7%), only one
Babesias pp. parasite was detected with 0.6% prevalence rate. The results
showed high prevalence rate of internal parasites (27.3%), Eimeria spp,
Hemoncus, Strongyloides, Monezia and Fachiola spp. eggs were detected
in fecal examinations with prevalence rates 12%, 8%, 2.6%, 4% and 0.7%
respectively. Statistical analysis for results was done and showed no
correlation between prevalence of blood and internal parasites with
origin, breed, sex and ages of sheep. A strong relationship was detected
between prevalence of blood parasites and body temperature of sheep.
VIII
الخالصة
من مختلف واليات السودان اجريت هذه الدراسة على مجموعات الضان القادمة الى الخرطوم
رأس من الضان 150 طالت الدراسة عدد قدو, بغرض الذبح لالستهالك المحلى والتصدير
مسالخ ثالثة منالنيل االبيض والقضارف تجمعت فى, دارفور, القادمة من واليات آردفان
بطفيليات الدم الصابة ا هدفت هذه الدراسة الى تقصى معدل 0المختلفةمدنها فى الوالية
وعالقة بعض العوامل مثل درجة حرارة جسم الحيوان باإلصابة بالطفيليات، والطفيليات الداخلية
.آذلك تأثير ساللة وعمر وجنس الحيوان على القابلية لإلصابة بالطفيليات
بالنسبة % 14,7بمعدل % 15,3اظهرت النتائج ان معدل حدوث االصابة بطفيليات الدم قد آان
0بالنسبة لطفيل البابيزيا% 0,6لطفيل الثيليريا ومعدل
0
بواقع نسب بلغت % 27,3الدراسة اوضحت معدال عاليا لالصابة بالطفيليات الداخلية بلغت
, ليات االتية على التوالى الكوآسيديا لكل من الطفي% 0,7 و 4% -2,6% -8% -12%
0 والفاشيوالمونيزيا, سترونقلس, هيمونكس
0
اشارت نتائج التحليل االحصائى للمعلومات المدخلة الى عدم وجود عالقة بين الطفيليات
فيليات الدم ى عالقة قوية بين طلالكنها اشارت , عمر واصل الحيوان,جنس, المذآورة و ساللة
0سم الحيوانودرجة حرارة ج
IX
INTRODUCTION
Sudan is rich in its animal's resources. The country has an animal
population estimated at 40.468 million cattle, 49.797 million sheep,
42.526 million goats, 3.908 million camels, 37 million poultry and 110
thousands ton fishers (MARF 2005).In Sudan there are several breeds of
sheep, such as, Kabashi, Hamari, Shukri and Zagawi in north and western
Sudan, Watish in central Sudan and Nilotic sheep in southern Sudan.
Sudanese sheep comprise 31% of the total population of sheep in the
Arab region (AOAD, 1998) and they are raised in different parts of the
country for their meat, milk, and hides. Exports of live sheep and mutton
contribute significantly to the national income from foreign exchange
which was estimated to be US$ 109 million annually in 1998. Sheep also
have religion and social importance. They play an important role in
public health because they could be a source for several zoonotic diseases
transmuted to man, such as, Brucellosis and T.B.
Sheep production in Sudan faces many problems including infectious
diseases caused by bacterial, viral, and parasitic agents. Bacterial and
viral diseases have almost been brought under control either by drug
therapy or vaccination. Parasitic diseases, however, have largely been
neglected primarily because they do not often cause acute faetal disease.
Blood parasites are living organisms which inhabit on blood and feed on
its constituents or nutrients. The blood parasites are difficult to control
due to the resistance of some parasites to drugs, and there is no successful
vaccine against most of blood parasites due to several factors such as
antigenic variation and difficulties in propagation of these organisms in
artificial media.
The infection with blood parasites can be suspected from general
symptoms of diseases such as decrease in production, emaciation, loss of
X
appetite and jaundice. Animals also take time to reach the peak of
production after recovery.
Sheep may be affected by Trypanosoma. vicax, Trypanosoma.congolnse
and Trypanosoma.dimorphon thats cause Trypansomosis, or Theileria.
lestoquadri which cause malignant ovine Theileriosis, Babesia.motasi,
Babesia.ovis that cause ovine babesiosis. Prelarval stages for several
nematodes, the microfilaria, which appear in several diseases affect sheep
such as Elaeophoriasis (filarial dermatitis in sheep), Thelasiasis (eye
worm), Neurofilariasis, Cerebrospinal nematodiasis (lumber paralysis).
Helminthes parasites are known to prevail in this country (Gagoad and
Eisa (1968), Eisa and Ebrahim (1970), Elbadawi et al (1978) and Atta
Elmannan (1983). Helminthes of the gastrointestinal tract are major cause
of reduced productivity in ruminants throughout the world (Holmes
1987). In general the effect of parasitic diseases on livestock include
mortality losses, condemnation of meat, weight loss, depreciation of
animal's products and reduced resistance to other diseases as well as
expenditure on drugs. Also they cause anemia, Economic effects the
damaged of the skin due to ticks and flies bites, costs of treatment,
prevention and control of parasites and vectors.
Therefore the objectives of this study are:
1- To detect blood and internal parasites of sheep brought to Khartoum
state in ante-mortem examination as a reflection of the common parasitic
infections in the production areas.
2- To examine the effect of geographic origin of sheep in occurrence of
parasitic infections.
3- To detect the prevalence of parasitic infections in different age groups.
4- To suggest a feasible strategy for control of parasitic infestation in
sheep herds.
1
CHAPTER ONE LITERTURE REVIEW
1.1 Sheep Breeds and Their Distribution in Sudan:
The estimated Sudanese national sheep flock is 49.797 million
head (MARF, 2005). Sudan sheep are conventionally classified on the
basis of morphology and distribution into four main groups: Sudan
Desert, Sudan Nilotic, Sudan Arid Upland and Sudan Equatorial Upland
(Mcleory, 1961; Wilson and Clarke, 1975). Fused ecotypes from non-
systematic crossbreeding at the boundaries of the ecozones have also
been recognized.
More than 65% of the sheep in Sudan are of the Sudan Desert type (Ovis
aries) (Sulieman et al., 1990), which is believed to be a descendant of
sheep of Egyptian origin (Ovis longipes). They are distributed north of
latitude 18N, extending eastward into Eritrea and westward into Chad
(Wilson, 1991) and are raised under pastoral system in the eastern and
western regions of the country. Sudan Desert sheep are further classified
into tribal subtypes, e.g. Hamari, Kabashi, Shenbali in North and West
Kordofan States (Mukhtar, 1985), Shugor, Dubasi and Watish in the
Central States (Sulieman et al., 1990) and Bourug in the Butana area of
eastern Sudan.
In recent years, the use of Sudan Desert sheep as an export commodity
has increased. In 1991/92, it contributed about $60 million to the national
foreign exchange earnings at an annual off take rate of 600,000 head
(LMC, 1992).
2
1.2 Sheep Meat Production
Sheep in Sudan play important role in production of meat for local
consumption and export to numerous countries, a total of 76.728.000
head of sheep were slaughtered in period (2000 to 2004), statistical
information on Tables (1-1), (1-2) and (1-3) (MARF, 2005).
3
Table (1-1) Slaughter sheep and meat production for local
consumption
2000-2004
year No of slaughter sheep
(000) head
Local consumption
(000) ton
2000 12545 138
2001 12909 142
2002 14041 154
2003 18495 222
2004 18738 225
Total 76728 881
Table (1-2) Estimation of sheep meat production for local
consumption and export (000) T 2000-2004
year for export Local cons. Total
2000 120 138 258
2001 120 142 262
2002 120 154 274
2003 60 222 282
2004 60 225 285
Total 480 881 1361
4
Table (1-3) Export of sheep meat (ton) 2000-2004
year meat production
2000 6157.8
2001 4855.2
2002 7113.8
2003 7837.11
2004 5570.9
Total 31534.81
5
1.3 Parasitic diseases of sheep
1.3.1 Sheep Blood Parasites
1.3.1.1 Trypanosomosis:
Until recently Trypanosomosis in sheep and goats was not ranked as an
important disease. Kramer (1966) reported that the disease in Nigeria was
of little importance in these hosts, Stephen (1970) and Finelle (1973)
stated that sheep and goats are seldom infected with Trypanosomosis
under natural conditions.
Later studies indicated that not only are these animals naturally infected
by this disease, but also high mortality can occur (Griffin and Allonby,
1979). Evidence was obtained from experimental infection that sheep and
goats act as reservoir and may be important in the transmission of
Trypanosomosis (Khasanov and Ivanitskaya, 1974 and Mahmoud and
Elmalik, 1978).
Thousands of sheep and goats were examined since 1942 in the upper
Nile province Sudan but only T. vivax was identified (Karib, 1961).
In Sudan, Boid et al. (1981) suggested the role of sheep and goats in
Kassala province as reservoir after he found antibodies against
Trypanosoma. evansi circling on there blood.
Osaer et al. (1999) stated that trypanosomosis seem to affect sheep and
goat health and production. Masiga et al. (2002) showed that mall
ruminants are susceptible to trypanosomosis and revealed anaemia and
reduction in body weight.
Infected animals usually look healthy and normal infections were often
chronic or sub clinical and were rarely detected because of low
parasitaemia and trypanosoma concentration, on the other hand Kalu et
al. (1986) observed that.
6
1.3.1.2 Blood parasites transmitted by ticks:
Ticks are regarded as an important external parasites in animals'
especially in tropical and sub tropical zones where they transmit most of
the serious diseases, among which the majority are blood parasites and
Reckittsea.
1.3.1.2.1 Sheep Theileriosis:
Theileriosis are tick borne protozoan diseases caused by Theileria spp in
cattle, sheep, and goats as well as in wild and captive ungulates (Radostits
et al., 2000). The diseases are characterized by fever and
lymphoproliferative disorders, which may be associated with leucopenia
and\or anemia (Radostits et al., 2000).
The important pathogen of sheep and goats is Theileria hirci (synonym
Theileria lestoquardi), the cause of malignant ovine theilerioosis
(Radostits et al., 2000). The disease is enzootic from North Africa
through the Middle East to India (Radostits et al., 2000). Theileria hirci
cause disease in sheep similar to Theileria annulata in cattle (Radostits et
al., 2000). In a recent Sudan outbreak involving eight flocks, 22% of the
sheep affected and all affected sheep were died within 3-6 days (Radostits
et al., 2000). Anemia, jaundice, and enlargement of lymph nodes are
characteristic, and both piroplasms and schizonts can be demonstrated in
smears of blood and tissues respectively. An indirect fluorescent antibody
test is available (Radostits et al., 2000). Parvaquone and buparvaquone
may be used to treat early cases (Radostits et al., 2000). Benign ovine
theileriosis is caused either by T. ovis or T. separate in Africa (Radostits
et al. 2000).
7
1.3.1.2.2 Sheep Babesiosis:
Babesosis are a group of tick born diseases caused by several species of
protozoa of the genus Babesia. These organisms are capable of infecting
all species of domestic animals, and also found in some wild animals,
which serve as reservoir of infection (Losos, 1986a). During infection
with babesia, the release of pharmacologically active substance and
destruction of erythrocytes play a major role in the pathogenesis of the
disease. However, the proportionate role of each varies with the
individual species of babesia (Soulsby, 1982). Anaemia is associated with
the emergence of the parasites from red cells. Often, however,
erythrocytes loss is attributed to the mechanical rupture of red cells by the
parasites although there have been no detailed studies of this in domestic
animals (Mohoney, 1977).
Babesia ovis in sheep and goats is distributed throughout tropical and
subtropical areas. Also in southern Europe and the former Soviet Union
(Soulsby, 1982). Its effect is less severe than other babesia species.
Although an acute phase characterized by fever, jaundice,
haemoglobinuria and anaemia may be seen, and in the chronic form of
the disease about 1% of the erythrocytes is infected (Soulsby, 1982).
Comprehensive reviews of the literature on Babesia and its infection had
been published by many authors, among them, Riek (1968), Mahoney
(1977) and Levine (1988).
Piroplasmosis in the Sudan was early reported in the beginning of the past
century, Babesiosis was reported in 1905 but little research was done by
(Hoogstral, 1956), FAO (1983), Abdoun (1984), Hashim (1984),
Mohammed and Yagoub (1990).
8
1.3.1.2.3 Anaplasmosis
Anaplasmosis is an acute or sub acute febrile disease of wild and
domestic ungulates. It caused by the Rickettsia. Anaplasma marginale,
Anaplasma Centrale and Anaplasma ovis, the former being more
pathogenic. It is characterized by progressive anaemia and occasionally
icterus (Losos, 1986b). Twenty species of tick have been shown to
transmit Anaplasma. Trnsovarial transmission occurs and insects (blood
sucking flies e.g. deer flies, stable flies) play a significant role in
mechanical transmission (Soulsby, 1982). Anaplasmosis causes
subclinical forms of the disease in sheep and goats but could be serious to
exotic cattle. In more chronic cases there is a sever anaemia and recovery
is slow. Control by vaccination has been attempted by several means for
many years. (Soulsby, 1982).
1.3.1.3 Filarial worms
These worms inhabit connective tissues and blood vessels, on the serosae
and in many other regions (Dunn, 1978).
The adult worms of genus Setaria are commonly found in the peritoneal
cavity of the final host, (Dunn, 1978). The microfilaria produced by
female circulate in the blood are unsheathed and measure 190 um 256
um. Setaria may incriminate in the etiology of cerebrospinal filariosis in
aberrant infections (Jones et al., 1997 and Mahmoud et al., 2004). Its
intermediate hosts in the tropical areas are mosquitoes of many genera
(Anopheles, Ades, Culex, etc.) (Soulsby, 1982).
1.3.2 The internal parasites that affect sheep
In most sheep-raising areas, internal parasites (i.e. worms) are usually the
primary disease affecting sheep and lambs (Susan 2006). Sheep are more
susceptible to internal parasites than most other types of farm livestock.
9
Their small fecal pellets disintegrate very easily thus releasing the worm
larvae onto pastures (Susan 2006). They graze close to the soil surface
and to their feces. They are slow to acquire immunity. It takes 10 to 12
months for most lambs to develop immunity to parasites. Sheep also
suffer a loss of immunity at the time of lambing, which does not restore
itself until approximately four weeks after lambing (Susan 2006). Heavy
stocking rates and insufficient pasture rest periods further contribute to
the incidence of parasitic disease in sheep and lambs. Internal parasites
tend to be much less of a problem under range-type conditions where
sheep do not graze the same pasture twice in the same grazing season.
They are also less of a problem in arid regions, because parasites require
moisture for their development (Susan 2006). In the past, sheep producers
relied heavily on anti-parasitic drugs, called "anthelmintics" to control
internal parasites in their flocks. But the long-time use and in some cases
misuse of these drugs has resulted in parasites that have become
increasingly resistant to anthelmintics. Drug resistance has been
documented in all three drug families and is most commonly reported
with ivermectin and the benzimidazoles. In the U.S., few anthelmintics
are FDA-approved for use in sheep and lambs, and no new drugs are
likely to be developed. As a result, producers must develop more
integrated programs for controlling parasites, which do not rely
exclusively on drug therapy (Susan, 2006).
10
Table 1.4 Internal Parasites that affect sheep and goats (Soulsby, 1982) Clinical signs Ideal Conditions for
Development Life cycle Site Common name Genus and species
Blood loss (Anemia), Edema ("Bottle Jaw"), Weakness Wool breaks, Sudden death
warm, moist summer rainfall
18 to 21 days
Direct Abomasum Barberpole worm Wire worm
Haemonchus contortis
Production loss, Lack of appetite Diarrhea, Weight loss, Decreased wool production.
cool, moist 20 days Direct Abomasum Medium or brown stomach worm
Ostertagia circumcincta
Black scours, Reduced appetite Production loss, Ocassional death
warm, moist < 21 days Direct Abomasum Small intestine
Bankrupt worm Hair worm
Trichostrongylus
Weight loss, Diarrhea, Inflammation between toes
warm, moist 7-9 days Direct Small intestine
Common threadworm
Strongyloides papillosus
Loss of appetite Diarrhea Weight loss Decreased wool growth
cool, wet winter rainfall
20 days Direct Small intestine
small intestinal worm
Coopera spp.
Usually sub-clincial Diarrhea, loss of appetite, weight loss
cool, wet 20 days Direct Small intestine
threadneck worm
Nematodirus spp.
Usually no signs of infection. Coughing, fluid in lungs if disease is severe. Pneumonia
cool, wet 5 weeks Direct Indirect (snails, slugs)
Trachea and bronchi
lungworm hair lungworm
Dictyocaulus filaria Muellerius capillaris
Heavy infestations may result in unthriftiness and GI disturbances
Wet 6 weeks
Indirect(pasture mites)
Small intestine
tapeworm Moniezia spp.
11
Liquid diarrhea Off feed, depression Death
cool, wet Overcrowding
< 21 days Direct Small intestine.
coccidia Eimeria spp.
Diarrhea Dry 6-12 weeks
Direct Caecum whipworm Trichuris ovis
Unthriftiness, Diarrhea Blood loss, Anemia Sore feet
warm, most 1-2 months
Direct Small intestine
hookworm Bunostomum phlebotomum
Damage lining of small intestines cool, wet winter rainfall
5 weeks Direct Large
intestine nodule worm Oesophagostomum
Hindquarter weakness Ataxia, Paralysis Blindness
cool, wet 82-91 days
Indirect (snails, slugs)
central nervous system
meningeal worm deer worm brain worm
Paralaphostrongylus tenius
production losses Death Organ condemnation
Wet 8-12 weeks
Indirect (snails, slugs)
Liver liver fluke
Fasciola hepatica
12
1.3.2.1 Prevalence of Gastrointestinal Helminthes of Sheep in Africa
In Egypt Shawakt et al (1994) examined 250 abomasums of sheep
slaughtered in Cairo abattoir; the examination revealed that 43.7% of
these were harboring single or mixed nematode infections.
Trichostrongylus spp, Haemonchus contortus and Oestertagia spp, were
identified in the study with prevalence rate of 28.9, 22.2, and 17.18%
respectively. Abd-Rabo et al (1993) examined gastrointestinal tracts of
sheep from Kafr-Elshih governorate, Egypt; He encountered 9 species of
nematodes (Trichostrongylus axei, Strongyloides papilosus, Haemoncus
contortus, Ostertagia trifurcta, Parabonema skrjabini, Nematodirus
spathiger, Trichuris ovis, Chabertia ovina and Oesophagostomum
columbianum). The frequency of nematode infection in the abomasums,
small and large intestine were 21.67, 21.67 and 36.67 respectively.
El Azazy (1990) examined 96 abomasums from sheep and goats at
Zagazig abattoir, Sharkia province, in 1986 and 1987 he observed that
adult Trichostrongylus axei was the most numerous followed by adult
Haemoncus contortus.
In Nigeria; Fakae and Chiejina (1993) conducted a survey on
traditionally reared west African Dwarf sheep and goats in the eastern
Nigeria for over 12 months period during 1987 to 1988. They reported
that the most prevalent nematodes were Haemoncus contortus and
Trichostrongylus colubriformis and which usually occurred together in all
nematode infected animals. Their combined prevalence rates ranged from
90% to 100%. On the other hand, Cooperia curticei and
Oesophagostomum columbianum were present in relatively small
numbers.
Earlier Fakae (1990) studied the epidemiology of helminthes infections in
west African Dwarf sheep and goats in the savanna area of eastern
Nigeria for 12 months, the infections observed involved Haemoncus
13
contortus, Trichostrongylus spp., Taenia hydatigena metacestodes, O.
columbianum, Strongyloides spp., Cooperia spp. And Gaigeria
pachyscelis with a prevalence rates of 87.1, 63.8, 30.2, 22.4, 18.8, 17.2,
and 6% repectivaly. Anene et al. (1994) carried out a survey of
gastrointestinal parasites of 948 small ruminants in south eastern Nigeria
in the dry and rainy seasons; they reported that Strongylys (mainly
Haemonchus) was the most prevalent gastrointestinal parasites in sheep.
The prevalence rate reported in the dry season was 39.8% while that of
the wet season was 63.7%. Onyali et al., (1989) studied patent infections
of Strongyloides papillosus in lambs under one week of age and it was
suggested that either the short generation interval or prenatal infection
was the cause. Worm egg counts taken at monthly intervals indicated
ranges from 100-1000 eggs per gram (e.p.g) of feces.
In Ethiopia Bekele et al., (1992) conducted post-mortem examination on
122 gastrointestinal tracts of sheep. In their study, they reported rates
ranging from 66.7% to 100% for Dictyocoulus filarial and 64% to 100%
for Trichostrongylus colubriformis, low prevalence rates for
Trichostrongylus axei, Haemoncus contortus, Oesophagostomum
columbianum, Bunostomum. Trigonocephalum and Trichuris. Srjabini
were reported. Njau et al., (1990) also investigated the prevalence rate of
gastrointestinal parasites of sheep in that country, the parasites found
were Coccidia, Haemoncus contortus, Trichostrongylus colubriformis,
Trichostrongylus axei, Ostertagia spp., Trichuris. Ovis, Chabertia Ovina
and Faschiola hepatica. Lemma (1998) found a seasonal pattern of
Trichuris ovis in sheep, and showed that the seasonal variations were due
to humidity (rain).
In Mauritania,Jacauiet et al., (1995) performed 647 faecal eggs counts
and 53 necropsies on sheep and goats originating from three sites of the
Sahelian region. The examination revealed that Haemoncus contortus,
14
Oesophagostomum columbianum and Stilesia globipunctata were the
most prevalence species.
In Kenya; Ndarathi et al., (1989) examined a total of 1412 animals from
three Masai groups for parasites, their study showed that between 60% to
70% of the sheep and goats were infected with gastrointestinal parasites,
and they stated that Strongylosis was the most prevalent gastrointestinal
infection allowed by coccidian, while prevalence of other parasites was
less than 6%. In another study Ndarathi (1992) reported that prevalence
of Haemoncus contortus, Trichostrongylus spp. And Oesophagostomum
spp. Were 91.1, 6.4, and 1.7% respectively.
Pandey (1990) examined 304 abomasums of sheep grazing on natural
pasture in Highveld, Zimbabwe; Haemoncus contortus was found in 70%
the organs examined. He observed that the worm burden increased during
the rainy season and was followed by a decline with low worm load
throughout the dry season.
In Zaire, Chartier et al.,(1990) examined carcasses of sheep, and reported
that the most frequent species were Haemoncus contortus,
Trichostrongylus colubriformis and Oesophagostomum columbianum
with prevalence rates of 70.1, 78.6, and 100% respectively.
1.3.2.2 Prevalence of Gastrointestinal Helminthes of Sheep in Sudan
In kordofan, Kassala, Darfur and Blue Nile provinces Gagoad and Eisa
(1968) examined 322 abomasums of sheep, their study showed that 80%
of the sheep harbored Haemobcus contortus. They reported that the
incidence rate in kordofan, Kassala, Darfur and Blue Nile was 83, 73.5,
and 75% respectively. Eisa and Ebrahim (1970) examined gastrointestinal
tracts of sheep obtained from Elobied, they reported the occurrence of
Haemoncus contortus, Trichostrongylus colubriformis, Strongyloides
papillosus, Oesophagostomum columbianum, Chabertia ovina, Cooperia.
15
pectinata, Trichuris ovis and Monezia expansa. Haemoncus contortus
was found to be the most prevalent species.
Elbadawi et al., (1976) conducted a study of helminthes parasites in 140
sheep carcasses in the southern region of the country. They reported the
dominance of Paramphistomum spp. Followed by Cysticercus.
tenuicollis, Faschiola gigantica and Schistosoma bovis. Elgezuli et
al.,(1978) carried out a survey of helminthes parasites of cattle, sheep,
goats and camels at Kassala province, they examined 341 large intestines
of goats and 66 of sheep. Their study showed that 11.7% of goats
harbored Skrjabinem ovis, while non of the sheep harbored this parasite.
Elbadawi et al., (1978) studied the incidence of helminthes parasites of
sheep slaughtered in the western provinces. A total of 1397 carcasses
were examined, they encountered eight genera of helminthes parasites
vise tow genera of trematodes (Paramphistomum spp. and shistosoma.
ovis), three genera of cestodes and larval cestodes (Avitellina spp.
Monezia expansa and Hydated cyst), and three genera of nematodes
(Trichuris ovis, Oesophagostomum colmbianum and Haemoncus
contortus )
The highest incidence was for Haemoncus contortus, Schistosoma bovis
and Oesophagostomum clombianum with a rate of 45.5, 44.5 and 39.5
respectively. The incidence of Trichuris ovis, hydated cyst, Monezia
expansa and Avitellina spp. was 20, 12, 9 and 3% respectively. They
showed that the maximum combination of genera found in one animal
was four in their checklist of helminthes in Sudan. Eisa et al., (1979)
reported helminthes in sheep in the Sudan during the period 1902-1975.
They reported 20 genera of helminthes parasites 5 genera of trematodes
namely (Faschiola gigantica, Schitosoma bovis, Paramphistomum spp.
Dicrocoelium spp. and Cotylophoron cotylophorum), 6 genera of
Cestodes (Avitellina spp., Monezia expansa, Monezia benedeni, Stilesia
16
hepatica, Cystecercus tenuiocollis, Hydated cyst , Coenurus cereberalis ,
Coenurus serialis), and 9 genera of nematodes (Bunostomum spp.,
Chabertia ovina, Cooperia pectinata, Gaigeria pachyscelis, Haemoncus
contrtus, Trichuris ovis, Oesophagostomum columbianum, Strongyloides
papillosus and Trichostrongylus axei ).
Atta Elmannan (1983) investigated the gastrointestinal parasites of sheep
and goats in Sennar district (central region) by means of microscopical
and post mortem examination. He found eggs of 4 genera of parasites
during faecal examination, this comprised Trichostrongylid spp., Monezia
expansa, Strongyloides papillosus, and Trichuris spp. the incidence of
parasites in sheep was 83.9%. where incidence of infection with one
species was the highest (43.9%) and with four species was the lowest
(3%), he revealed that Trichostrongylus axei was the dominant species
during examination of gastrointestinal tracts.
Atta Elmannan et al., (1983) studied the prevalence of Oesophagostomum
columbianum in sheep in Sennar district, they examined a total of 28
gastrointestinal tracts for adults worms. They showed that 21 were
infected with a prevalence of 75%.
Ahmed and Elmalik (1997) investigated the prevalence of Nematodes in
sheep brought to Khartoum from different localities of Sudan, four genera
of Nematodes were identified from faecal culture, these include, H.
contortus, Strongyloide papillosus, Oesophagostomum spp., and
Trichostrongylus spp., with a prevalence rates of 56.3, 36.6, 3.7 and 3.4%
respectively. The highest of infection was observed during the rainy
season 85% compared with a rate of 35.6% during the winter.
Ghada (2000) studied the prevalence of gastrointestinal helminthes of
sheep from central Kordofan and White Nile state. She examined 1005
faecal samples from sheep, she showed that presence of different
helminthes eggs, which include, Trichostrongylus, Strongyloide
17
papillosus, Trichuris spp., Monezia expansa, Monezia bendeni and
Paramphistomum spp., with a highest prevalence rates in rainy season.
1.4 Transmission
1.4.1. Transmission of blood parasites:
1.4.1.1 Cyclic transmission:
In this mode of transmission the parasites are capable to develop
cyclically in side the vector.
Trypanosome in Africa are mainly transmitted by Glossina species (tsetse
fly) in which trypanosome are capable to develop cyclically in the
digestive tract of the fly. Different trypanosome species develop in
different regions of the digestive tract of the fly, these are Trypanosoma
congolense, T. vivax, T. brucei, T.simiae, T. suis (Hoare, 1972).
The piroplasms-infected erythrocytes are ingested by a clean tick (Larva
and nymph) when it feeds and piroplasm released which differentiate into
sexual stages in the gut of the tick (Schein, 1975). The parasite multiplies
to schizont after inoculation of sporozoites with saliva of infected ticks
into the vertebrate host and invades different leukocytes (lrvin et al.,
1982).
1.4.1.2 Mechanical transmission:
In this mode of mechanical transmission, the parasites are taken up with
blood and survive for short time in the mouth part of insect (Hoare,
1970).
Tabanidae and other biting flies were incriminated for this type of
transmission in area far from tsetse main belt and in the countries out side
Africa. Hoare (1957) put forward hypothesis that Trypanosoma vivax had
become established in Mauritius and the new world by adapting
completely to mechanical transmission. He further argued that
18
Trypanosoma evansi originated from Trypanosoma brucei by similar
adaptation to mechanical transmission. Domizio (1930) and Spena (1948)
reported the occurrence of Trypanosoma vivax in Eritrea and central
Ethiopia, which are tsetse free areas. They both considered tabanids and
Stomoxid flies to be the vectors. Also Buxton (1955) mentioned that
Tabanids and biting muscids are important vectors of trypanosomes in
some tsetse free parts of Africa. Several authors wrote and conducted
studies on the role of tabanids and other biting flies in epidemiology of
Nagana and Surra. Roeder et al. (1984) described an incidence of acute
Trypanosoma vivax infection in cattle in high lands of Ethiopia where the
weather is too cold for tsetse survival. Outbreaks of Trypanosoma evensi
in cattle and buffaloes in India were reported to increase with the
increasing numbers of Tabanus spp. and Stoomoxys spp. In Vietnam,
Phung and Pham (1995) dissected biting flies and identified considerable
rate of T. evesi infection in tabanids, Stomoxys calcitrans and Heamatebia
exigua. Hussein et al. (1991) reported Atylotus spp. as vectors of
Trypanosoma evensi in camels in Saudi Arabia. Desquesnes and Dia
(2003) demonstrated the ability of one of the most common tabanids
found in Africa, Atylotus agrestis, to transmit T. vivax mechanically to
cattle.
1.4.2 Internal parasites transmission
1.4.2.1 Direct transmission
Nematode can be transmited directly in case of pasture contamination by
ingestion of free L3 (infective stage) such as Trichostrongyloid and
Strongyloid, however infection sometimes can happen by larval
penetration of the skin or by ingestion of the eggs containing a larva
(Radostits et al., 2000).
19
1.4.2.2 Indirect transmission
In case of nematodes, the first two moults usually take place in an
intermediate host and infection of the final host is either by ingestion of
intermediate host or by inoculation of the L3, when the intermediate host
such as blood sucking insect feeds (Radostits et al., 2000).
Trematodes are transmited by the snails as intermediate host, the infective
stage (cercaria, metacercaria) emerge from snail and swim to contaminate
the pasture.
The typical life cycle of cestodes is indirect with one intermediate host.
1.5 Diagnosis
1.5.1 Diagnosis of sheep blood parasites:
1.5.1.1 Diagnosis of sheep Trypanosomosis:
Clinical diagnosis of individual animals is indicated (Uilenberg, 1998)
but not confirmative (OIE, 1996).
Trypanosomoses can be diagnosed by direct parasitological, serological
or molecular techniques.
1.5.1.1.1 Parasitological methods:
These methods include examination of fresh drop of blood under cover
slip as a wet smear, stained thin and thick film. Thos are specific
techniques but theire sensitivity is relatively low, as parasitaemia is
generally low and fluctuating. Therefore, negative results do not always
mean that the animal is not infected. Negative test should be repeated
before establishing final diagnosis (OIE, 1996). More sensitive
parasitological method depends on the concentration of trypanosomes in
the buffy coat by microhaematocrit centrifugation techniques (Woo,
1970). This technique is efficient and may detect as few as 5
trypanosomes\ml (Kalu et al., 1986).
20
The relative efficiency of these several methods of diagnosis may vary
between trypanosomes species, the chance may be improved by used dark
ground \phase contrast and concentration techniques (Murray et al.,
1977). Also in this method measuring packed cell volume is indication of
the degree of anaemia (Woo, 1970; Murray et al., 1977; Brown et al.,
1990; OIE, 1996).
1.5.1.1.2 Serological methods:
The antibodies detection by several techniques has been tried for
diagnosis of trypanosomes. At the present the in direct fluorescence
antibody test (IFAT) allows detection of species-specific antibodies (OIE,
1996), the method had been widely applied for diagnosis for bovine
trypanosomosis in Africa (Luckins, 1992).
The enzyme linked immunosorbent assay (ELISA) has been used to
detect infection in camels (Luckins, 1999), buffalo and cattle (Payne et
al., 1991). Desquesnes et al., (1996) reported that Ag ELISA is an
important tool for epidemiological surveys.
1.5.1.1.3 Molecular biology techniques:
The principle of the molecular tests is the demonstration of the
occurrence of sequences of nucleotides, which are specific for
trypanosome subgenus, species or even type or strain (Uilenberge, 1998).
Polymerase chain reaction (PCR) is based on the use of an enzyme, DNA
polymerase enzyme. The technique was used to be an efficient tool for
estimation of the prevalence of African trypanosomosis (Solano et al.,
1999).
21
1.5.1.2 Diagnosis of tick born diseases
1.5.1.2.1 Provisional diagnosis:
The simples' diagnostic method is case history, clinical signs, post-
mortem findings and knowledge of disease and vector distribution (OIE,
2000), despite the fact that clinical picture of the disease is not
pathognomic (Lossos, 1986a). The clinical signs include fever,
enlargement of peripheral lymph nodes, difficult breathing, frothy nasal
discharge (Boulter and Hall, 2000).
Diarrhoea, lacrimation, dullness, haemoglobinuria in case of babesiosis,
recumbency and death may occur within two to three weeks post
infection (Gill et al., 1977; Uilenberg, 1981). Post mortem findings
include subcutaneous and pulmonary oedema, petichial hemorrhages on
various organs.
1.5.1.2.2 Laboratory diagnosis:
By Geimsa stained blood or tissue smears in order to detect schizonts in
lymph nodes and impression smears, while piroplasms appear in blood
smears (Soulsby, 1982; Norval et al., 1992).
1.5.1.2.3 Serodiagnosis:
The most suitable and commonly used serum antibody assay has been the
indirect fluorescence antibody test (IFAT) (Burridge 1971; Burridge and
Kimber, 1972; Burridge et al., 1974; Goodeeris et al., 1982). The test has
been widely used in epidemiological studies in different African countries
including Sudan (FAO, 1983).
Recently the enzyme linked immunosorbant assay (ELISA) is widely
applied in detecting circulating parasites-specific antibodies, antigens and
immune complexes (Dolan, 1989). The test has many advantages
compared with (IFAT).
22
1.5.1.2.4 Molecular techniques
Usage of molecular tools based on DNA hypridisation to detect parasites
were discussed by many authors. D,Olivera et al. (1995) reported the
detection of T. annulata in cattle using (PCR).
Two integrated approaches were developed to detect several Thieleria or
Babesia spp, in one assay (Figueroa et al., 1993; Allsopp et al., 1993).
Using these approaches multiple species can be detected in one assay
without performing independent PCR for each parasite (Gubbels et al.,
1999). PCR combined with reverse line blot (RLB) hybridization
(Gubbels et al., 1999) is used to detect and differentiate all known
Theileria and Babesia spp. on bases of their differences in 185 subunit
rRNA gene sequences (Gubbels et al., 1999). A similar approach has
been followed for detection and differentiation of Anaplasma spp.
Targeting the 165 rRNA gene (Jongejan, 2003).
1.5.1.3 Diagnosis of microfilaria
Detection of microfilaria in blood can be done by concentration method
after centrifugation of blood in micro haematocrit tube or in wet smear
covered with a cover slip. The larva may be detected by the snake-lie
movement under low magnifications (Jain, 1986). The recommended
method for stained blood film consists of adding 1.0ml of fresh blood to
10ml of 2% formalin solusion and centrifuged at 1,000-1,500 rpm for few
minutes. The sediment is examined microscopically as a wet smear after
being mixed with an equal volume of 1:1000 methylene blue (Jain, 1986).
A drop of serum in slide covered with cover slip examined for viable
larvae (Jain, 1986).
23
1.5.1.4 Diagnosis of internal parasites
1.5.1.4.1 Gross examination
Feacal samples should be examined for any intact specimens such as
Moniezia spp. segment and Oesophogostomum species adults.
Examination of the smear only indicates the presence of infection
regardless of its quantification (Dunn, 1978).
1.5.1.4.2 McMaster Technique
Mc Master Technique depends on the examination of a precise volume of
suspension of faeces in floatation solution, to allow an estimation of the
number of eggs and larvae present in a sample. The natures of solution
vary according to the animal origin of the suspected material and mixing
performed in various ways. The essential equipment is a slide that
consists of two layers of glass separated by a known distance and having
on the upper layer a ruled squire of known area (King, 1976).
1.5.1.4.3 Concentration methods
Concentration depends on specific gravity of the eggs and is not reliable
in estimating the intensity of an infection, and can be achieved by
sedimentation or floatation (King, 1976).
1.5.1.4.3.1 Sedimentation
The parasite eggs do not float, but deposit in the solution either by slow
natural precipitation of faecal suspension or by the use of centrifugation.
This method is relevant to fascioliasis, schistosomiasis and
paramphistomiasis (King, 1976).
24
1.5.1.4.3.2 Flotation
In this method the specific gravity of the solution is higher than the
specific gravity of the eggs. Thus the solution used is at saturation or
semi-saturation such as sodium chloride and sugar (sucrose). The method
is used for nematodes.
1.6 Control
1.6.1 Control of sheep Trypanosomosis:.
1.6.1.1 Treatment of Trypanosomosis:
By using trypanpcidal drugs for the treatment and or prevention is the
most widely accepted method for controlling the disease (Tacher, 1982;
Losos, 1986).
Chemoprophylactic drugs are used in highly tsetse infested areas and the
only difference from curative drugs that in case of prophylaxis the drug
persist longer (Uilenberge, 1998).
The available and common trypanocidal drugs are Diminazen-acturate
(Berenil), Quinapyramine sulphate and chloride (Antrycide) and
Isometamidium (Samorin).
1.6.1.2 Vector control:
In vector control several methods were applied, these are including bush
clearance to minimize the density of flies by destroying the tsetse shelter
and resting sites (Ford, 1970; Finelle, 1974; Walker, 1986). This method
is seldom used now (Finelle, 1974). Elimination of game animals in order
to starve tsetse flies by reducing the source of food (Ford, 1970). Due to
the world concern to conservation wild life, the method no longer used.
25
1.6.1.3 Use of insecticides:
Application of insecticides like chlorinated hydrocarbons chiefly DDT
and dieldrin in the past (Finelle, 1974), organophosphrus and pyrethroids
are applied in ground or aerial spraying. This is most effective method
(Allsopp, 1984). Synthetic pyrethroid is also applied by dipping or used
as pour on, depending on the particular insecticide used, ticks and other
ectoparasites may also be reduced. The use of traps and insecticide-
impregnated targets with or without attractants is a method to suppress
tsetse populations (Challier and Laveissiere, 1973; Vale, 1974, 1993;
Brandl, 1988; Bauer et al., 1995).
1.6.1.4 Biological control:
Recently application of sterile insect technique has been achieved
successfully in Zanzibar by systematic releases of sterile male among the
target population (Feldmann and Hendrichs, 2001). This method is very
specific and not polluting (Uilenberg, 1998).
1.6.1.5 Tabanids control:
The most suitable method to control tabanids is the use of chemical
attractants to trap males, this help to reduce the disease out side the tsetse
belt (Mohammed et al., 2000).
1.6.2 Control of Ticks and tick-borne diseases
1.6.2.1 Treatment
1.6.2.1.1 Chemotherapy
Usage of ox tetracycline and chlortetracycline are affective in arresting
macro- and micro schizonts formation in the beginning of the infection of
Theileriosis and also used for treatment of anaplasmosis (Sousby, 1982).
26
Diminazene aceturate (Berenil) at a dose of 3.5 mg\kg B.W
intramuscularly in case of Babesiosis and combined with oxyteteracycline
15mg\kg B.W. for theileriosis treatment.
Halofuginone lactate at 1.2 mg\g B.W. given orally shown to be highly
effective for theileriosis (Schein and Voiget, 1979).
Parvaquone (Clexon) is effective at 10 mg\kg B.W. administered
intramuscularly in two injections with 48 hours interval (Gille et al.,
1984; MacHardy and Morgan, 1985; Musisi et al., 1985; Mehta et al.,
1987 and Unsuren et al., 1988).
Buparvaquone (Butalex) is twenty times more effective than parvaquone,
it is given at 2.5 mg\kg B.W. (McHardy et al., 1985).
Imidocarb (Imizol) is used as chemotherapy and also eliminate
anaplasmosis from carrier animals (Roby and Mazzola, 1972) cited by
Soulsby (1982).
1.6.2.1.2 Chemoprophylaxis
By subcutaneous inoculation of ground suspension of infected tics with a
subsequent intramuscular injection of oxytetracycline (Malik et al.,
1987).
1.6.2.2 Vaccination
Vaccination against tropical theileriosis is established in some parts of the
world namely Israel, Turkey, Iran and Iraq (Soulsby, 1982 and Losos,
1986) attenuated vaccines obtained by serial passage of schizont infected
lymphocyte, and this provided a significant protection (Srivastava and
Sharma, 1977; Broun, 1979). Development of vaccine against tropical
theileriosis in cattle and malignant ovine theileriosis in sheep in Sudan is
needed to be evaluated experimentally (Jongejan, 2003).
27
1.6.2.3 Control of ticks:
Using acricides in dips for large herds and hand spray or used as pour on
(Drumond, 1976; Losos, 1986a).
1.6.3Treatment of microfilaria
Many broad spectrum anthelmintics have a high efficiency against
Microfilaria (Drudge et al., 1969), one of those drugs, is Ivermectin, it is
a drug of choice to eliminate Microfilaria in horses (Pollitt and
Holdworth, 1986) at 0.2mg\kg B.W.
Other drugs include Diethyl carbamazine a microfilaricidal in both man
and animals at a dose of 5-8 mg\kg B.W. daily for 21 days. Also systemic
corticosteroids are recommended (Cello, 1971).
1.6.4 Control of internal parasites
Fischer and Say (1989) explained that the control of gastrointestinal
parasites depends mainly on drug prophylaxis for eliminating the
parasites by regular treatment. The animal should be given antihelmentics
at the end of the rainy season in order to improve the adaptation of the
animal to harsh dry season conditions. A second treatment by
antihelmentics should be given at the end of the dry season so that the
infection of pasture by parasites at the time of the first rains can be
reduced.
On the other hand, Thursfiled (1996) described that the level of infection
with some nematodes can be reduced by mixed, alternate and sequential
grazing.
28
CHAPTER TWO
MATERIALS AND METHODS
2.1 Study sites description
The study was conducted in Khartoum State which is situated in Northern
Sudan between latitude 16°N and 14°N. The total area extends over
approximately 21,000 square kilometers.
Khartoum state contained three basic Towns (Khartoum, Khartoum North
and Omdurman), each of them is divided administratively into a number
of localities. One slaughter house was selected randomly from each town
to be the site for the study, Al Sahafa abattoir represented Khartoum,
Ghanawa abattoir represented Omdurman and Kuku abattoir represented
Khartoum North. The selection was done on the basis of the number of
animals slaughtered, as these are the largest in the three towns also the
animals are brought from all over the country to these slaughter houses
2.2 Sampling
Sampling was done according to Thrusfield (1995), the slaughter houses
were selected from Khartoum state (Khartoum, Khartoum North and
Omdurman). All animals in each slaughter house were sampled at the
time of the visit, this samples collection method called Cluster sampling
or Two-stage sampling method.
2.3 Study population
All sheep from different origins, in different age group and sex brought to
slaughter house at the time of visit were targeted as study population.
29
2.4 Samples collection
For blood and internal parasites detection, blood samples, faecal samples
were collected, tick infestation was observed, and body temperature was
taken, information on origin, breed, sex and age were recorded for each
animal.
2.4.1 Blood sample collection
A total of 150 blood samples were collected form the ear vein of sheep
for both thin blood smear and wet amount examinations. Samples were
placed in a cool box and transferred to the laboratory before processing
for parasitological examination.
2.4.2 Faecal samples collection
Fresh faecal samples were collected from the rectum of every individual
sheep in plastic vacutainer. The samples were labeled and immediately
transferred to the laboratory for faecal examinations.
2.4.3 Ticks observation Ticks were observed on individual selected animals according to the
presence or absence.
2.5 Parasitological examination
2.5.1 Wet blood mount:
One drop of fresh blood was placed on a slide, covered with a cover-slip
and examined microscopically for detection of motile parasites at 10×40
magnification.
2.5.2 Thin blood film:
Thin blood films were prepared on slides, dried and fixed with absolute
alcohol. Then these smears were stained with 5% diluted giemsa stain
30
solution for 45 minutes. Films were washed using distilled water, dried
and examined microscopically under oil immersion at 10×100
magnification for blood parasites detection.
2.5.3 Faecal examination
2.5.3.1 Flotation method
Two to three grams of the faeces were taken in a mortar, ground and
mixed thoroughly in a saturated sodium chloride solution. The suspension
was poured through a tea sieve into a beaker to remove the large particles.
The solution was poured into a small bottle until it was completely filled
to make a convex meniscus at the top. Then it was covered with a clean
grease-free cover slide. The cover slide was removed after 10 minutes
and placed on a clean slide to be examined under Low power 10 × 20
magnifications. The examination was done systemically to cover all the
cover slip.
2.5.3.2 Sedimentation
Two to three grams of the faeces were mixed with water and put in tubes.
the tubes were centrifuged three times for 5 minutes, each supernatant
fluid was removed and replaced each time. The deposits were taken and
placed on slides with covers slip and examined microscopically at high
power 10× 40 magnifications for detection of parasites ova.
2.6 Data analysis
Microsoft Excel (windows 2003) and state 6.0 for windows 98/95/NT
were used for data analysis. Chi-square (χ2) was used for assessing the
statistical associations of various factors for presence of blood and
internal parasites. Logistic regression model was employed to obtain the
31
odds ratio (OR) only for those factors which gave statistical significant by
using chi-square (χ 2).
If the odds Ratio was greater than one the factor could be a risk factor for
the presence of blood or internal parasites.
32
Table (2.1) Description of the study population
Origin
Breed
Sex
Age
Slaughter
House
No. of
animal
examined
White
Nile
Gadaref
Kordofan
Darfur
Kabbashi
Ham
ari
Baladi
Male
Female
< 1
1 - 2
> 2
Elsahafa
50
-
45
5
-
5
-
45
47
3
44
4
3
Ghanawa
50
-
-
26
24
35
14
-
14
9
11
28
9
Kuku
50
40
-
10
-
36
15
-
41
36
20
31
-
Total
150
40
45
41
24
76
29
45
102
48
75
63
12
33
Chapter Three
Results
The results showed that, the prevalence of blood parasites in
Khartoum state was 15.3% (n≡150) with 18% (n≡50), 16% (n≡50) and 12
% (n≡50) in Omdurman, Khartoum North and Khartoum respectively
(Table 3-1).
Also the prevalence of internal parasites was 32%, 28% and 22% in
Khartoum North, Omdurman and Khartoum respectively (Table 3-1).
Ticks presence observed was 16, 8% and 8% in Omdurman, Khartoum
and Khartoum North respectively (Table 3-1).
No motile parasites were detected (Table 3-1), high temperatures were
observed only in Omdurman with 6% prevalence rate (Table 3-1).
The highest prevalence rates was due to Theileria spp., 12%, 14% and
18% in Khartoum, Khartoum North and Omdurman respectively with
14.7% total prevalence (Table 3-2). Only one animal showing Babesia
spp was detected in Khartoum North (2% prevalence rate as 0.6% of total
rate) (Table 3-2). Tick infestation was observed at 8%, 16% and 8%
prevalence rates in Khartoum, Omdurman and Khartoum North
respectively, with 10.7% total prevalence rate.
On the other hand results of internal parasites indicated the presence of
protozoa, nematodes, cestodes and trematodes, (Eimeria, Hemoncus,
Strongyloide,, Monezia and Fachiola spp). Trophozoites or eggs were
detected in fecal examinations with prevalence rates 12%, 8%, 2.6%, 4%
and 0.7% respectively (Table 3-3).
Coccedia spp prevalence rate was the highest (10%, 16% and 10% in
Khartoum, Khartoum North and Omdurman respectively) (Table 3-3).
The prevalence of Heamonchus spp was 6%, 8% and 10% in Khartoum,
Khartoum North and Omdurman respectively (Table 3-3).
34
2%, 4% and 6% were the prevalence rates of Monezia spp in Khartoum,
Khartoum North and Omdurman respectively (Table 3-3). Strongyloides
prevalence was 4%, 2% and 2% prevalence rates in Khartoum, Khartoum
North and Omdurman respectively (Table 3-3). Fasciola was found in
only one sample from Khartoum North with 2% prevalence rate (Table 3-
3).
Statistical analysis showed no correlation between prevalence of blood
parasites and place of origin (χ2 = 3.7027, p=0.295), age (χ2 = 4.047, p =
0.132), sex (χ2 = 0.915, p = 0.339), breed (χ2 = 3.065, p = 0.216) and ticks
presence (χ2 = 0.640, p = 0.424) (Table 3-4).
Also there are no co relation between presence of internal parasites and
origin (χ2= 2.023, p = 0.568), age (χ2= 0.585, p = 746), sex (χ2=0.321, p =
0.571) and breed (χ2 = 0926, p = 0.629) (Table 3-5).
A strong association was found between presence of blood parasite and
temperature (t-test = -628.515, p = 0.000) (Table 3-6).
35
Table (3.1): Parasitic Burden of Animals Examined
Parameters
Khartoum
Location
Omdurman
Khartoum
North
Total
No of animal
examined
Body temp.
Normal
High temp.
Tick presence
Positive
Stained blood film
Blood parasites
Fecal exam
Sedimentation
method
Internal parasites
Floatation method
Internal parasites
50
100%
_
8%
12%
_
22%
50
94%
6%
16%
18%
_
28%
50
100%
_
8%
16%
2%
30%
150
98%
2%
10.7%
15.3%
0.6%
26.7%
36
Table (3.2) the prevalence of blood parasites in slaughter houses in
Khartoum state
Slaughter house
No. of
animal
examined
Prevalence %
Theileria spp Babesia spp
No. (%)
Elsahafa
Kuku
Ghanawa
Over all prevalence
50
50
50
150
6(12%) _
7(14%) 1 (2%)
9(18%) _
22(14.7%) 1 (0.6%)
37
Table (3.3): The prevalence of internal parasites in slaughter houses in Khartoum state
Slaughter
house
Eimeria spp
No. (%)
Heamonchus
spp No. (%)
Strongyloides
No. (%)
Monezia spp
No. (%)
Fasciola No.
(%)
Total
Elsahafa
Kuku
Ghanawa
5 (10%)
8 (16%)
5 (10%)
3 (6%)
4 (8%)
5 (10%)
2 (4%)
1 (2%)
1 (2%)
1 (2%)
2 (4%) 3 (6%)
_
1 (2%)
_
11 (22%)
16 (32%)
14 (28%)
Total 18 (12%) 12 (8%) 4 (2.6%) 6 (4%) 1 (0.7%) 41(27.3%)
38
Table (3.4): The relationship between presence of blood parasites and
origin, age, sex, breed and tick infestation.
Factor
Chi-square(χ2)
P-value
Origin
Age
Sex
Breed
Ticks
3.7027
4.047
0.915
3.o65
.640
0.295
0.132
0.339
0.216
0.424
39
Table (3.5): The relationship between presence of internal parasites
and origin, age, sex and breed.
Factor
Chi-square (χ2)
P-value
Origin
Age
Sex
Breed
2.023
0.585
0.321
0.926
0.568
0.746
0.571
0.629
40
Table (3.6): The association between presence of blood parasites and
animal body temperature
Factor
No of
animals
examined
SE
t-test
p-value
Temperature
150
0.503
-628.515
0.000**
**: highly significant (P< 0.01)
NB. Normal body temperature ranged 39ºc- 40 ºc according to Radostits et al (2000).
41
Chapter Four
Discussion
The study showed no Trypanosomiasis infection in the
samples examined. That agrees with different workers (Stephen, 1970
and Findle, 1973) who stated that sheep and goats are seldom infected
with trypanosomes under natural conditions. Khasanove and Tranitskaya
(1973), Mahmoud and Elmalik, (1978) established experimental infection
of Trypanosoma and showed that sheep and goats may act as reservoir
and may be important in the transmission of trypanosomosis, Karib
(1961) stated that thousands of sheep and goats were examined in the
Upper Nile Province but only T.vivax was identified. Boid et al (1981)
suggested the role of sheep in Kassala Province as reservoir after he
found antibodies against T. evansi circulating in their blood. On the other
hand the study revealed a higher prevalence of Thieleriosis compared to
Babesiosis. Radositits et al (2000) cited that in an outbreak of Thieleria
infection involving 8 flocks, 22% of sheep were affected and all of them
died within 3-6 days. Losos (1986) reported that Theileria hirci in Africa,
Asia and Europe causes enzootic diseases; The young lambs contract a
relatively mild form of the disease which renders mature animal immune;
The mortality rate in sheep is relatively low about (16%) in infected
cases; The distribution of T.ovis is comparable to the distribution of
T.hirci. In general piroplasmosis in Sudan was early reported in the
begining of past century and Babesiosis was reported in 1905, yet limited
research was done such as the work by Hoogstrsal (1956), FAO (1983),
Abdoun (1984) Hashim (1984) Mohamed and Yagoub (1984).
The results of the present study showed high prevalence rate of internal
parasites infection (Coccediosis, Monezia infection, Strongyloid
infection, Haemonchosis and Fsciolosis), the protozoa were the most
common and they belonged to the genera Eimeria spp. (Coccedia.)
42
Similarly, Osman, et al (1990), reported outbreaks of coccediosis among
sheep and goats in fattening centers around Khartoum state. Other
workers recorded the presence of internal parasites of sheep in Sudan, in
kordofan, Kassala, Darfur and Blue Nile provinces. Gagoad and Eisa
(1968) examined 322 abomasums of sheep, their study showed that 80%
of sheep harbored Haemonchus contortus. They reported that the
incidence rate in kordofan, Kassala, Darfur and Blue Nile was 83%,
73.5%, and 75% respectively. Eisa and Ibrahim (1970) examined
gastrointestinal tracts of sheep obtained from Elobied, they reported the
occurrence of H. contortus, T. colubriformis, S. papillosus, O.
columbianum, Chabertia ovina, Cooperia pectinata, Trichuris ovis and
M. expansa. H. contortus was found to be the most prevalent species.
This study revealed that there was no effect of sheep place of origin on
the prevalence of blood and internal parasites that might be due to
similarities of management conditions in various areas of origin, (White
Nile, Gadaref, Kordofan and Darfour). Also sheep in various locations
may meet in different occasions during seasonal migrations of herds.
Negative relationship was obtained between ticks infestation and blood
parasites infection. This could be attributed to the fact. That ticks dropped
during the period of travels.
Also the study revealed that there was no effect of breed on the
prevalence of blood and internal parasites (χ2= 0.005, p> 0.05). That
could be attributed to the fact that the animals examined were genetically
more than 65% of the sheep in Sudan are of the Sudan Desert type (Ovis
aries) (Sulieman et al., 1990), which is believed to be a descendant of
sheep of Egyptian origin (Ovis longipes). Therefore the so called breeds
may be types rather than distinct breeds. Sudan Desert sheep are further
classified into tribal subtypes, e.g. Hamari, Kabashi, Shenbali in North
and West Kordofan States (Mukhtar, 1985), Shugor, Dubasi and Watish
43
in the Central States (Sulieman et al., 1990) and Bourug in the Butana
area of eastern Sudan.
No correlation (χ2= 0.483, p> 0.05) was found in this study between sex
and presence of blood and internal parasites. Similar results were reported
by Flach et al. (1993), who stated that there was no relationship was
established between infection of engorged nymphs of ticks and sex of
host animal. Thus sex is not a determining factor in susceptibility to tick-
borne parasites. Both sexes graze in same under similar field conditions
which may explain the negative correlation between sex and internal
parasites.
This study was conducted in the hot season (April, May, June), when the
ova and egg and worm counts decreased, while both high faecal egg
output and high worm counts were observed during the rainy season. This
could be attributed to the suitability of environmental conditions of
moderate temperature and moisture prevailing during the rainy season
(Temp 28-31ºC; RH 37.5-70%) providing optimum requirements for
development of infective nematode larvae (Pandey, 1990; Onyali et al.,
1990; Agyei, 1991; Rahman, 1992). Both egg and worm counts decreased
at the end of the rainy season and this might be due to a self-cure
phenomenon as these animals have been sensitized for several months
during the rainy season and subsequently lost their worm burdens (Altaif
et al., 1980; Altaif and Issa, 1983; Chaudhry et al., 1988). This decrease
continued throughout winter and summer and was probably induced by
dryness. This fact is in conformity with observation of several authors in
some African countries such as Nigeria. Okon and Enyenihi (1977),
Ogunsusi (1979), and Chiejina and Fakae (1984) studied pasture
infectivity with trichostrongylid larvae in that country and showed that
the dry season was unfavourable for pre-parasitic development and
survival of nematode larvae. In Tanzania, Connor et al. (1990) reported
44
that egg output declined and remained low during the dry season due to
lack of moisture. In addition Chiejina et al. (1989) reported that the dry
season is responsible for the rapid drying out of faecal pellets leading to
death of parasite eggs and larvae. On the other hand sheep brought to
Khartoum state came for local and export marketing, which means
owners select healthy, youngest and fit animals. Also this study was
conducted on relatively small number of sheep (150) compared with total
number brought to the state annually for export and local consumption.
According to MARF (2005) in the last five years from 2000 to 2004,
more than 76 millions head of sheep were slaughtered for local
consumption and 480 thousands ton were exported. With the above
mentioned in this study the results showed that high prevalence of blood
parasites (15.3%) and (27.3%) with regards to for internal parasites,
which are very harmful for man and sheep, with regards to helth and
economy, there is direct loss from expected condemnations of affected
parts and decrease in animal proteins available for human consumption so
it is vital to:
1- Pay more attention to sheep blood and internal parasites,
epidemiology and control nation wide.
2- Conduct similar surveys for blood and internal parasites, to cover
all animals brought from various states of Sudan to Khartoum for
local and international consumption.
3- Apply practical methods of prevention and control such as use of
chemotherapeutic control, vector control and continuous veterinary
monitoring in the slaughter houses especially in ante- mortum
inspection.
4- Draw attention to the exported sheep and try to minimize losses in
production due to the parasites.
45
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