PREVALENCE OF GASTROINTESTINAL HELMINTHS IN

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PREVALENCE OF GASTROINTESTINAL HELMINTHS IN EXTENSIVELY
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MANAGED PIGS IN MEKELLE CITY, TIGRAY NORTHERN ETHIOPIA
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Zewdneh Tomass*1, Ekwal Imam1, Taddese Dejenie1 and Kidane Weldu2
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1, Mekelle University, College of Natural and Computational Sciences, Department of Biology,
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Po.Box:
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(*tom_zewde@yahoo.com)
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2, Mekelle University, College of Veterinary Medicine, Department of Veterinary Medicine,
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231,
Tel:
+251
348400381,
Fax:
+251
34401090/
P.Box:231, Tel: +251 0914 02 73 98, Fax: +251 34401090/ +251 34419403
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+251
34419403,
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ABSTRCT
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BACKGROUND: Poor environmental sanitary facilities coupled with extensive pig
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management are reported to be risk factors of infection of the animals with variety of
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gastrointestinal parasites in developing countries. On the other hand, pigs play a substantial role
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as potential reservoir hosts of zoonotic intestinal parasites.
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METHODS: Fresh fecal samples were collected from pigs of different ages and microscopically
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examined for eggs of gastrointestinal helminths after flotation and sedimentation techniques.
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RESULTS: Out of 207 pigs, 176 (85%) were infected by at least one helminth parasite.
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Helminth infection was more common in pigs with 3-6 months of age. Highest mean occurrence
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of infection was observed in pigs in “Endasilasie”site . However, occurrence of infection was not
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statistically significant between male and female pigs in all sites. Ascaris spp was the most
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encountered parasite followed by Hyostrongylus spp and Fasciola hepatica.
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CONCLUSITONS: Apart from helminth induced morbidity on the infected animals, the
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potential of Ascaris spp of pigs to infect man and vice versa coupled with unhygienic
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environmental condition may complicate the epidemiology and control of ascariasis in the study
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areas. Hence, proper pig husbandry and adequate environmental hygiene is crucial to prevent
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intestinal helminthiasis among pigs and potential public health hazards.
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Key words/Phrases: Extensive pig husbandry, Gastrointestinal parasites, Zoonoses, Tigray,
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Ethiopia
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INTRODUCTION
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The occurrence of parasitic helminth infections are markedly influenced by the type of pig
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husbandry used (Nansen and Roepstorff, 1999). Extensive production of pigs is most practiced in
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resource-poor communities of developing countries including Africa. Lower costs associated
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with the overall management, easy availability of household or municipal garbage as feed and
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possibilities to get better nutrition through scavenging than limited variety of feed in intensive
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farming initiate farmers in developing countries to prefer extensive pig production. Hence, 70-
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95% of pig farming sector use traditional extensive production system in developing countries
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(Lekule and Kyvsgaard, 2003).
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However, poor environmental sanitary facilities coupled with extensive management of pigs are
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reported to be risk factors of infection of the animals with variety of helminth and protozoan
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gastrointestinal parasites (Nansen and Roepstorff, 1999; Honeyman, 2005; Weka and Ikeh, 2009;
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Lai et al., 2011). For instance, highest counts of gastrointestinal helminth parasites including
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Oesophagastomum
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quadrispinulatum, Trichostrongylus axei, Strongyloides ransomi, Hyostrongylus rubidus and
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Physocephalus sexalutus have been identified among pigs raised under extensive production
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system in Kenya (Nganga et al., 2008). Tamboura et al. 2006 reported gastrointestinal nematode
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parasites of various species in scavenging pigs in Burkina Faso. In Ghana, pigs grown by
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households under extensive management scheme are reported to be infected with gastrointestinal
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helminth fauna including Metastrongylus salmi, Physocephalus sexalatus, Ascarops strongylina,
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Brachylaemus suis, Paragonimus suis, Globocephalus urosubulatus and Schistosoma suis
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(Permin et al., 1999). Semi-extensively managed pigs are reported to harbor Taenia solium, in
dentatum,
Trichuris
suis,
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Ascaris
suum,
Oesophagastomum
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Nigeria (Gweba et al., 2010). Pigs rose under smi-intensive and extensive production scheme in
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and around Holeta, Ethiopia, were reported to harbor intestinal helminthes, Ascaris suum and
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Oesophagostomum spp (Abdu and Gashaw, 2010). On the contrary, Roepstorff and Nansen,
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1994 reported decrease in number of helminth species and their infection levels as pig production
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systems are shifted from non-intensive to highly intensive ones.
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Pigs infected with gastrointestinal parasites had poor feed conversion rate and delays in
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achievement of market weight. Furthermore, Infection of pigs with gastrointestinal parasites
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results in condemnation of organ parts or entire carcasses causing economic losses (Hale and
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Stewart, 1998). In addition, pigs infected with intestinal parasites may act as source of zoonoses
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through contaminating the environment with intestinal parasites contained in their feces (Uysal et
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al., 2009).
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In Ethiopia the population of pigs has shown slight increment during the years 1980-2000
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(Knips, 2004). However, Pig rising is at its infancy in the country with a total population
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estimate of about 1900 (CSA, 2004). Recently small scale pig production is being practiced in
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urban areas of Ethiopia (Abdu and Gashaw, 2010). However, the production system practiced in
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the country is manly extensive whereby pigs are allowed to scavenge on household wastes at
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backyards and municipal garbage at the edge of towns (Abdu and Gashaw, 2010; Personal
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observation); such production system coupled with pigs’ voracious feeding behavior causes
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infection of the animals with gastrointestinal parasites of various species. Nevertheless, there is a
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paucity of data regarding prevalence of gastrointestinal helminths in extensively managed pigs in
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Ethiopia in general and Tigray Region in particular (Abdu and Gashaw, 2010). Therefore, this
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study was initiated to investigate infection prevalence of gastrointestinal helminths among
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extensively managed pigs in selected Kebeles (the smallest administrative units of cities) of
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Mekelle city, Tigray, Northern Ethiopia.
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MATERIALS AND METHODS
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Study areas
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This study was carried out in selected Kebeles of Mekelle city. Mekelle is the capital city of
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Tigray Region located 780 km north of Addis Ababa, the capital city of Ethiopia (Fig. 1). Its
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geographic location is 13° 32’ N and 39° 33’ E. It has an average altitude of 2200 meters above
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sea level with a mean minimum, mean maximum and mean average monthly temperatures of
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8.7, 26.8 and 17.6° C, respectively (Kibrom, 2005). Amount of rainfall in Mekelle is on average
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about 600 mm, and more than 70% of it falls between July and August, followed by long dry
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season (Kibrom, 2005). Mekelle has an estimated total population of 215,546 (CSA, 2008).
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Urban agriculture is a common practice in Mekelle (Ashebir et al., 2007). “Kwiha”, “Aynalem”,
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“Midregenet”, “Mariam Dahan”and “Debri” are among the suburban villages of Mekelle where
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subsistence agriculture is practiced. About 9248 households depend on subsistence urban
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agriculture in the aforementioned environs of Mekelle. The livestock population of Mekelle
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includes a total of 49,519 bovine, 274 camels, 5384 ovine, 6993 coprine, 61, 324 poultry, and
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7696 equine. Pigs are recently introduced into Mekelle and raised by few households for market.
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The livestock management types that are practiced in Mekelle include extensive, intensive and
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semi-intensive (MZAO, 2011).
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Some households in “Kwiha”, “Endasilasie”, “Hadinet” and “Adi Haqi” Kebeles of Mekelle are
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engaged in extensive pig razing, therefore, these sites were selected for the study. “Kwiha” is
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located at the southern periphery of Mekelle city close to Alula Aba Nega air port; “Endasilasie”
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is situated at close distance to Mekelle University main campus on the way to down town;
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“Hadinet” is located at the south east of Mekelle city; “Adi-Haqi” Kebelle is located close to the
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Martyrs' Memorial Monument of Tigrai People Liberation Front (TPLF).
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Collection of fecal samples
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Fresh fecal samples were collected as soon as dropped by pigs of different ages before touching
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the ground. Fecal samples were collected early morning when households release pigs from their
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pens. About 5 grams of the captured fecal sample was put in screw cap bottles containing 10%
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formalin. The fecal samples were then transported to the parasitology laboratory of the
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Department of Biology, Mekelle University, on same day and stored at 4 °C until processed.
Fig.1: Map of Mekell City showing study sites
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Examination for gastrointestinal helminthes
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Flotation
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Three gram of each fecal sample was mixed with 50 ml of 0.4g/ml sodium chloride (flotation
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fluid) using mortar and pistil; the resulting fecal suspension was poured through a tea strainer
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into a beaker; the suspension was then poured from the beaker into a test tube leaving a convex
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meniscus at the top; a cover slip was then carefully placed on top of the test tube and the test tube
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was let to stand for 20 minutes, then the cover slip was carefully lifted from the tube together
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with a drop of fluid adhering to it and immediately placed on a glass slide for microscopic
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examination (Bayou, 2005).
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Sedimentation
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To detect helminth eggs which do not float well in the sodium chloride solution such as Fasciola
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spp, simple sedimentation technique was carried out. For this purpose, 3 g of feces was put in a
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conical flask and mixed with 30 ml of water; the mixture was then sieved through a tea strainer
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into a beaker, transferred into a centrifuge tube and centrifuged at 1500 rotation per minute for 3
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minutes; the supernatant was then discarded, the sediment was mixed with 1% of methylene blue
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and examined under the microscope using 40  objective lens (Bayou, 2005).
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Statistical analysis
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Comparison of mean occurrence of gastrointestinal parasites among the sites was determined by
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one-way analysis of variance (ANOVA) using SPSS for windows, version fifteen. Chi-square
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test was used to see if there is any difference in occurrence of gastrointestinal parasites in pigs
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with respect to age and site (Das, 2009).
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RESULTS
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Out of 207 pigs, 176 (85%) pigs were infected by at least one helminth, with an overall
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prevalence rate of 85% (Table 1). The mean occurrence of helmminth infection in pigs among
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the four Kebelles in Mekelle was significantly different (p=0.18) [Table 2]. Occurrence of
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intestinal helminths was not significantly different between male and female pigs ( X 2 =0.34).
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The occurrence of intestinal helminths was more common in pigs with ages ranging from 3-6
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month (P > 0.05) (Table 3).
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Table 1. Number and infection rates of pigs from four Kebeles of Mekelle, Ethiopia, January -
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March, 2012
No. of pigs
Occurrence of
Occurrence of mixed
No. (%)
Kebeles
sampled
single infection
infection
positive
Hadnet
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19 (A12, H 6, F 1)
7(A&H), 3(A & F)
29(81)
18(A&S), 10(A&F),
Adhaki
95
42(A 29, H 8, F 5)
11(A,H&F), 6(H&F)
87(92)
Kwiha
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21 (A 19, H 2)
3 (A,H&F), 5(A&H), 4(A&F)
33(72)
4( A&H), 2(H&F), 2( A&F),
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169
170
171
172
Endasilassie
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Totals
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18 (A 10, H 8)
1(A,H&F)
27(90)
176 (85%)
A= Ascaris suum, H = Hyostrongylus spp, F= Fasciola hepatica
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Table 2. Mean occurrence of helmitnh infection among pigs at Kebeles in Mekelle, Ethiopia,
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January -March, 2012
Mean
Kebeles
No. of pigs
occurrence of
sampled
infection
Hadnet
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1.11  0.12
Adhaki
95
1.51  0.08
Kwiha
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1.17  0.11
Endasilasie
30
1.23  0.12
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Table 3. Occurrence of intestinal helminths in pigs with respect to age groups in Mekelle,
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Ethiopia
Age ranges (in
Occurrence of
months)
parasite *
3-6
55
6-12
27
12-18
49
18-30
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*, X 2 = 17.04
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On the other hand, the distribution of intestinal helminths in pigs among the sites was
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significantly different (P > 0.05) [Table 4]. Ascaris suum was most frequent in “Kwiha” ( X 2 =
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2.4) followed by “Adhaki” ( X 2 = 0.73), “Endasilasie” ( X 2 = 0.32) and “Hadnet” ( X 2 = 0.10).
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Hyostrongylus spp is most frequent in “Kwiha” ( X 2 = 1.9) followed by “Endasilasie” ( X 2 =
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1.4), “Hadnet” ( X 2 = 0.16) and “Adhaki” ( X 2 = 0.003). Fasciola hepatica was most frequent in
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“Adhaki” ( X 2 =1.98) followed by “Hadnet” ( X 2 = 1.15), “Kwiha” ( X 2 = 0.78) and
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“Endasilassie” ( X 2 = 0.32) [Table 4].
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Table.4. Distribution of intestinal helminths in pigs at different Kebeles in Mekelle, Ethiopia,
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January-March, 2012.
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Sites
Midre-
Total
Parasites
Kwhiha Endasilassie Genet
Adhaki (%)
Ascaris spp
38
17
22
68
145 (53)
Hyostrongylus spp
11
15
13
43
82 (30)
Fasciola hepatica
7
5
4
32
48 (17)
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DISCUSSION
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In the present study 85% of the pigs were found to be infected with at least one intestinal
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helminth parasite. Apart from other factors, scavenging feeding habit of pigs might have
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contributed for such a high rate of helminth infection in the study sites. Ascaris spp was found to
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be the most common helminth in all age categories of pigs examined in the present study. This
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result is in agreement with findings of similar studies in other developing countries including
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Africa (Nsoso et al., 2000; Tamboura et al., 2006; Yadav and Tandon, 1989). On contrary to our
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finding, Tiwari et al., 2009 reported no evidence of A. suum infection in pigs in Grenada, West
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Indies suggesting existence of variation in epidemiological occurrence of A. suum infection in
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pigs in developing countries of different continents. However, A. suum is naturally a parasite of
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pigs; recent reports indicate human cases of A. suum infection (Arizono et al., 2010). The
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potential of A. suum to infect and grow to adult stage in the human host might be due to the fact
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that it shares similar protein molecules with that of Ascaris lumbricoides for which man is the
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natural host (Alba et al., 2009). There are even hypothesis claiming A lumbricoides and A. suum
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to be single species except with the name Ascaris lumbricoides Linnaeus 1758 taking priority
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over Ascaris suum Goeze 1782. (Leles et al., 2012). This may imply free ranging pigs in the
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present study areas may act as potential reservoir hosts human ascariasis.
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Hyostrongylus spp was the second most encountered parasite with 30% prevalence rate in pigs
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examined in the present study. This result is higher than the prevalence rate of Hyostrongylus spp
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reported in extensively managed pigs in particular districts of Kenya, Burkina Faso and Uganda
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(Nganga et al., 2008; Tamboura et al., 2006; Nissen et al., 2011). Furthermore, no evidence
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Hyostrongylus spp prevalence was reported by a similar study around Holetta, Ethiopia (Abdu
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and Gashaw, 2010). On the contrary, Permin et al. 1999 reported higher rate (60%) of
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Hyostrongylus spp in pigs in selected villages of upper east region of Ghana.
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Fasciola hepatica is the least encountered parasite that is, 17% among different age groups of
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pigs in the present study. This result is consistent with the infection prevalence of F hepatica in
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pigs reported from the rural Chilean provinces (Apt et al., 1993). On the other hand, Bornay-
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Llinares et al. 2006 detected F hepatica in slurry of pigs of different age groups in Spain. Factors
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that contribute for the spread of F. hepatica among livestock in a particular locality in
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developing countries may include presence of infected animals, presence of snail intermediate
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hosts and ability of the parasite to colonise and adapt to new hosts. Presence of snail intermediate
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hosts and presence of infected animals in an area may again be facilitated by practice of irrigated
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agriculture and movement of infected animals, respectively from endemic areas (Mas-Coma et
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al., 2005). Therefore, as F hepatica is one of the plant-borne zoonotic trmatodes, its occurrence
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in pigs in the present study might be due to the use of metacercaria contaminated vegetables and
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pasture from irrigated fields as an additional feed source.
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The mean occurrence of helminth infection in pigs among the four Kebelles in Mekelle was fond
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to be significantly different (p=0.18); this may be due to the difference in hygiene profile of
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foraging grounds of pigs among the Kebelles. Some of the pig foraging grounds observed during
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our field visit includes the garbage damping site of a military camp in “Kwiha”; garbage around
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Kebelle 17 market in“Endasilasie”; garbage damped in and around unfinished houses in
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“Hadnet” and garbage damped along the northward length of the municipal wastewater drainage
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canal in “Adi-Haqi”. On the other hand, There was no statistically significant difference
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( X 2 =0.34) in the infection rate of intestinal helminths between male and female pigs. It is
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observed during the field visit that both sexes of pigs feed voraciously on garbage and it seems
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that both sexes of the animals have equal chances of being infected with the parasites. This result
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is in agreement with the previous study in Holeta, Ethiopia (Abdu and Gashaw, 2010).
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Furthermore, in the present study occurrence of intestinal helminths was more common in pigs
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with ages ranging from 3-6 month (P > 0.05). The possible reason for more infection prevalence
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of intestinal helminths in young age groups of pigs in this study may be due to the lower immune
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status. However, Abdu and Gashaw, 2010 reported that there is no statistically significant
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difference in the infection rate of gastrointestinal parasites among the different age groups of
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pigs in Holeta, Ethiopia.
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CONCLUSION AND RECOMMENDATION
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Three intestinal helminth species were found to infect scavenging pigs in different Kebelles of
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Mekelle City. Ascaris spp was found to be the most common intestinal helminth. The
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possibilities of Ascaris spp of pigs to infect man and vice versa coupled with unhygienic
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environmental condition may complicate the epidemiology and control of ascariasis in the study
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areas. In the present study extensively managed pigs are also reported to harbor Fasciola
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hepatica suggesting their potential as source of infection for other livestock. Therefore, further
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investigations are required to determine the level of environmental contamination by intestinal
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parasites contained in pig feces and the possible impact of parasitic infections of pigs on public
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health in Mekelle, Ethiopia.
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ACKNOWLEDGEMENTS
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We would like to acknowledge the Department of Biology, Mekelle University, for laboratory
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facilities. We are also grateful to Mr. Haile Misganaw, Mr. Teklemedhin G/Hiwot, Mr. Seret
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Teklu and Miss Medhin Weldu for their unreserved assistance during field fecal sample
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collection. Pig owners in the study areas are highly acknowledged for their cooperation during
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sample collection.
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