Gastrointestinal helminths of local backyard chickens in North Gondar Administrative Zone, Ethiopia

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1 Gastrointestinal helminths of local backyard chickens in North Gondar Administrative Zone, Ethiopia W. MOLLA 1 *, H. HAILE 1, G. ALMAW 2, W. TEMESGEN 3 1 Department of Veterinary paraclinical studies, Faculty of Veterinary Medicine, University of Gondar, P.O. Box 196, Gondar, ETHIOPIA. 2 National Animal Health Diagnostic and Investigation Center, P.O. Box 04, Sebeta, ETHIOPIA. 3 Department of Veterinary epidemiology and public health, Faculty of Veterinary Medicine, University of Gondar, P.O. Box 196, Gondar, ETHIOPIA. *Corresponding author: mollawassie@yahoo.com SUMMARY A cross-sectional study was conducted on local backyard chickens in three selected districts of North Gondar Administrative Zone (Dembya and Gondar in midland, and Wogera in highland) to estimate the prevalence of gastrointestinal helminth infections and identify the involved parasite species. A total of 260 chickens were purchased, sacrificed and their gastro-intestinal tracts were examined for adult helminth parasites. The overall gastrointestinal helminth prevalence was 79.62% and mixed helminth infections were found in 56.52% of birds. Nematodes (3 species) were recovered in 157 (60.38%) chickens, whereas cestodes (7 species) were found in 142 (54.62%) birds. Raillietina echinobothridia (29.62%), Raillietina tetragona (12.31%) and Hymenolepis cantaniana (10.00%) were the most prevalent cestodes identified while the recovered nematodes included Ascaridia galli (39.23%), Hetrakis gallinarium (39.62%) and Dispharynx nasuta (3.46%). Significant difference in the occurrence of cestodes was observed among the 3 selected districts, the birds from the midland areas being more frequently infected. No significant effects of age, sex or body condition on the helminth susceptibility were evidenced in the local backyard chickens. These results show that gastrointestinal helminths are highly prevalent in local backyard chickens in North Gondar and the identification of the predominant cestod and nematode species is required for establishing appropriate control and prevention strategies. Keywords: Chickens, backyard, gastro-intestinal helminths, prevalence, cestodes, nematodes, North Gondar, Ethiopia. RÉSUMÉ Helminthes gastro-intestinaux chez les poulets de race locale en élevage traditionnel dans la zone administrative Nord de Gondar, Ethiopie Une étude épidémiologique a été conduite sur les races locales de poulets en élevage traditionnel issues de 3 districts particuliers de la zone administrative Nord de Gondar (Dembya et Gondar en plaines et Wogera en altitude) afin de déterminer la prévalence des infestations par des helminthes gastro-intestinaux et d identifier les espèces de parasites impliquées. Les helminthes adultes gastro-intestinaux ont été recherchés sur 260 poulets de race locale. La prévalence globale a été de 79,62 % et des infestations multiples ont été observées dans 56,52 % des oiseaux infestés. Des nématodes (3 espèces distinctes) ont été mis en évidence dans 157 poulets (60,38 %) alors que les cestodes (7 espèces distinctes) ont été identifiés chez 142 oiseaux (54,62 %). Les cestodes les plus fréquemment identifiés ont été Raillietina echinobothridia (29,62 %), Raillietina tetragona (12,31 %) et Hymenolepis cantaniana (10,00 %) et Ascaridia galli (39,23 %), Hetrakis gallinarium (39,62 %) et Dispharynx nasuta (3,46 %) ont constitué les 3 espèces de nématodes identifiées dans cette étude. La prévalence d une infestation par les cestodes est apparue significativement dépendante de l origine géographique, les oiseaux issus des plaines étant plus souvent infectés. Aucun effet significatif de l âge, du sexe ou de l état corporel sur la sensibilité aux helminthes des poulets en élevage traditionnel n a été détecté. Ces résultats montrent que les poulets de race locale en élevage traditionnel de la région Nord de Gondar sont souvent parasités par des helminthes gastro-intestinaux et l identification des principales espèces de cestodes et de nématodes est un pré-requis indispensable à l établissement de stratégies de contrôle et de prévention des helminthiases. Mots clés : Poulets, élevage traditionnel, helminthes gastrointestinaux, prévalence, cestodes, nématodes, Gondar Nord, Ethiopie. Introduction In developing countries, over 6 billion poultry are kept under different production systems. In Africa, about 80% of the chicken populations are found in traditional production system [8]. In Ethiopia, chickens are widespread and almost every rural family owns chickens, which provide a valuable source of family protein and income [21]. The total poultry population of Ethiopia is estimated at 38.1 million and approximately 99% are raised under the traditional backyard system with little or no inputs for housing, feeding or health care [1, 4, 6, 14, 21]. Chickens in backyard production are with constant risk of infestation by both ecto- and endoparasites since they get little to no feed supplementation thus, resorting to scavenging and foraging for feed to meet their nutritional requirements. In this production system, helminth infections are ubiquitous and even when they occur in low numbers, may result in subclinical disease [12, 15]. Helminth infestations are associated with unthriftness, poor growth due to poor feed conversion rate, reduced egg production and fertility and in acute worm infestations lead to death [1, 15, 19]. Gastrointestinal tract (GIT) helminthiasis of poultry is a parasitic disease caused by nematodes (round worms), cestodes (tape worms) and trematodes (flat worms) that have different predilection site in different segments of gastrointestinal tract in birds [23]. An accurate identification

2 GASTRO-INTESTINAL HELMINTHS IN CHICKENS FROM NORTH GONDAR 363 of these parasites at species level may give directions to control measures aiming to eliminate the intermediate hosts and therefore to break the life cycle [17]. The prevalence and intensity of helminth infections may be influenced by several factors, such as distribution of intermediate hosts and/or their infection rate and the number of infective parasite eggs or larvae. Host factors such as age, sex and breed can also influence helminth infection [12]. Absence of biosecurity and scavenging habits of chickens in free range conditions can also contribute to helminth infections [17, 19]. In addition to disease, lack of feed, housing, poor management, and to lesser extent financial problems are the main constraints with this production system in Ethiopia [14]. Symptomatic diagnosis of poultry helminthiasis is generally very difficult since the infections are often chronic [13]. A reliable diagnosis can only be performed by accurate identification of individually recovered parasites. Therefore, careful and complete necropsy of the representative members of the flock is essential [11]. In Ethiopia, gastrointestinal helminthiasis is an important poultry disease, causing great economic loss. Limited surveys carried out at different times and places in Ethiopia indicate the existence of high prevalence and wide distribution of poultry gastrointestinal parasites in backyard chickens [1-3, 6, 22, 24]. In the North Western part of Ethiopia, there is no enough information except that of AWOKE [2] who reported 92.4% prevalence of helminthiasis in and around Bahir Dar. More importantly, there was no such a study conducted before in North Gondar Administrative Zone and the status of the disease was not known in this area. However, it is well understood that before any control attempt of poultry gastrointestinal parasites in backyard flocks it is necessary to know what parasites are present and to evaluate the importance of the parasite population. Thus, it is necessary to generate relevant information that helps to design control strategy. Therefore, the objectives of the present study were to determine the prevalence of gastrointestinal helminth infection and to identify different helminth parasites in the gastrointestinal tracts of chickens managed under traditional backyard system of production in North Gondar Administrative Zone, Ethiopia. Material and Methods STUDY DESIGN Study area The study was conducted in North West of Ethiopia since October 2010 to March 2011on backyard chickens obtained from three selected districts of North Gondar Administrative Zone, Wogera (highland), Gondar town (midland) and Dembya (midland), representing two agro-ecological zones. The study area lies approximately 550 m (in Western lowland) to m (Semen Mountain in North) above sea level and the average annual rainfall varying from 880 mm to mm that is characterized by a mono-modal type of distribution. The mean annual minimum and maximum temperatures are 10 C in the highland and 44.5 C in the lowland, respectively. Geographically the area lies between N latitude and E longitude. Study animals Apparently healthy local chickens (n = 260, 137 females and 123 males) were bought from local open air markets in the respective study areas. The birds were categorized into two age groups, namely growers and adults. The age of birds was determined subjectively based on the size of crown, length of the spur, appearance of the beak and flexibility of the xyphoid cartilage [5]. The body condition of birds was also determined subjectively following the technique explained by GREGORY and ROBINS [9] and was categorized into 3 groups as poor (p), medium (m) and good (g) body score both for adults and growers. Sensitive weight balance was used to measure the live weight; growers weighing less than 400 g, between 400g and 600g and more than 600 g and adults weighing less than 650 g, between 650g and 800g and more than 800 g were considered as poor, medium and good respectively. The poultry management patterns involving local chickens in the study areas were entirely free ranging system. Study design cross-sectional type of study design was used for the study and chickens of both sex and different age groups were purchased. The age, sex, geographical location and body conditions of chickens were recorded as test variables during data collection of target chickens. Three visits were made to Wogera and Dembya and 30 chickens were bought during each visit. Four visits were made to Gondar town and 20 chickens were bought during each visit. All visits to the indicated sites were made during the local market days. A total of 260 chickens were bought from the three districts. Birds were transported to Gondar University and were necropsied at Faculty of Veterinary Medicine, Gondar, Ethiopia. The recovered parasites were fixed in universal sampling bottle containing 70% ethyl alcohol. POST-MORTEM ANALYSES Post-mortem examination was performed following the procedure indicated by PERMIN and HANSEN [16] and PHIRI et al. [18]. The chickens were starved overnight and were killed by cervical dislocation: the head was grasped with a hand shake grip and then thumb fingers were extended under the throat. The feet and wings grasped together with the other hand and the bird stretched until the head separated from the cervical vertebrae. Post-mortem examination was carried out immediately following the euthanasia. The killed bird was placed on the table and an incision was made in the abdominal skin just below the tip of the breast cartilage. The cut extended around the body on each side and the upper edge of the skin grasped to peel the skin over the breast. The skin on the abdomen where the legs join the body was incised using surgical scissor and then, a hand placed on each leg and pressed to dislocate the femoral joints. An incision on the abdominal muscle was extended below the tip of the breast bone toward the point of wing attachment on each side. The breast was then pushed toward the head and then head and shoulder joints were dislocated and finally the breast was removed from the carcass. Liver,

3 364 MOLLA (W.) AND COLLABORATORS heart and spleen were removed to expose the digestive tract. A transverse incision cranially to the proventriculus is made and the whole intestinal tract was removed in a caudal direction. To remove the whole intestinal tract a transverse incision was made 1-2 cm cranial to the cloacae. The oesophagus and the crop are removed by separation from the other tissue and pulled in a cranial direction. The gastrointestinal tract (GIT) was then separated into 4 pieces; the oesophagus and crop in one piece, gizzard with proventriculus, caeca and the rest of intestine. Each part was opened and its contents were emptied into separately labelled beakers. Any visible worm (s) to naked eye during opening of the intestine parts were picked up using thumb forceps and the recovered helminths were shifted to labelled universal sampling bottles containing 70% ethyl alcohol. The mucosa of the intestine parts was washed to remove any adhering parasites. The beakers containing the contents of the parts were filled with tap water and allowed to settle. The supernatant was decanted and the beaker re-filled with water. The process was repeated several times and then, the content was sieved, emptied on Petri dish. Any worm noticed was picked up and added to sampling bottle containing 70% ethyl alcohol keeping the parts separate. All the adult worms were identified directly under light microscope (4x and 10x magnifications). Cestodes were identified based on the morphology of the scolex (first criteria), morphology of the strobilla (the way how one proglottid is attached to the other), size of the parasite and sometimes morphology of the genital organs in cases when the scolex was detached. Nematode parasites were identified considering the size of the parasite, the presence or absence of spicules (in males), oesophageal bulb and the predilection site of the parasites. In general, identification of both cestodes and nematodes was done using helminthological keys described by SOULSBY [19] and PERMIN and HANSEN [16]. STATISTICAL ANALYSIS Collected data were first entered into a Microsoft Excel spreadsheet and analyzed using Stata 11 software. Descriptive statistical analysis was used to summarize and present the data collected. The helminth prevalence was calculated as the number of chickens harbour helminth parasite in their GIT, divided by the total number of birds examined. The degree of association between each risk factor and parasite infection was assessed using the Pearson Chi-square (χ 2 ) test. For all analyses, a P- value of less than 0.05 was considered as significant. Results As shown in Table I, the overall prevalence of gastrointestinal helminths in backyard chickens was high (79.62%). There was no statistically significant difference in the prevalence rates of gastrointestinal helminth infections among the three selected districts; however, a relatively higher infection was observed in the chickens from Gondar town (82.5%) and Dembya (82.22%) representing midland regions. A relatively lower prevalence was observed in the chickens from Wogera (74.44%) representing highland region (Table I). Nematodes were the most predominant parasites recovered in 60.38% (157/260) of the birds whereas cestodes were identified in 54.62% (142/260) birds and no trematode parasite was evidenced in any bird. Young grower birds (84.61%) were more often infected with helminth parasites than adults (78.36%) but difference according to the age was not significant. Multiple infections were also observed in large number of infected birds (56.52%, i.e. 117/207) irrespectively of the study areas, sex, body condition, and age of chickens; they often associated 2 species (76 cases, 64.96%), scarcely 3 species (34 cases, 29.06%) and rarely 4 or more species (7 cases, 5.98%). Among the 260 examined chickens, cestodes were identified in 142 birds (54.62%). The most frequently identified specie was Raillietina echinobothridia with a prevalence of 29.62%. Two other species, Raillietina tetragona and Hymenolepis cantaniana, were also largely evidenced in 12.31% and 10.00% infected chickens respectively, while the prevalences of Amoebotania sphenoides and Choenotaenia infundibulum remained low (below 5.00%) and Raillietina cesticillus and Hymenolepis carioca were rarely observed (prevalences: 1.15% and 0.77% respectively) (Table II). In addition, mixed infections with two and more cestod parasites were relatively common and were observed in 21 cases. Moreover, the cestod prevalences have significantly varied according to the geographical origin of birds, those from the midland districts (Gondar and Dembya) being more frequently infected, particularly with the 3 predominant species (R. echinobothridia, R. tetragona and H. cantaniana), than those from the highland (Wogera) district (P < 0.05) (Table II). On the other hand, no statistically significant difference in cestod prevalence was observed according to the age, sex and body condition as summarized in Table III. A total of 157 (60.38%) birds were infected by different nematode parasites. Mixed infections with more than one nematode species was a common phenomenon, present in 57 cases. The most prevalent nematode parasite in the current study was Hetrakis gallinarium (39.62%, found in 103 chickens) followed by Ascaridia galli (39.23%, found in 102 chickens), while Districts Examined Infected Prevalence (%) Wogera (highland) Gondar (midland) Dembya (midland) Total TABLE I: Prevalence of gastrointestinal helminths in traditional backyard chickens (n = 260) from three districts of North Gondar Administrative Zone, Ethiopia.

4 GASTRO-INTESTINAL HELMINTHS IN CHICKENS FROM NORTH GONDAR 365 Cestod spp. Infected (prevalence) Total (n = 260) Wogera (n = 90) Gondar (n = 80) Dembya (n = 90) Raillietina echinobothridia 77 (29.62%) 14 (15.56%) 30 (37.50%) 33 (36.67%) Raillietina tetragona 32 (12.31%) 8 (8.89%) 13 (16.25%) 11 (12.22%) Raillietina cesticillus 3 (1.15%) 1 (1.11%) 2 (2.50%) 0 (0.00%) Choenotaenia infundibulum 10 (3.85%) 2 (2.22%) 3 (3.75%) 5 (5.56%) Hymenolepis cantaniana 26 (10.00%) 7 (7.78%) 10 (12.50%) 9 (10.00%) Hymenolepis carioca 2 (0.77%) 0 (0.00%) 2 (2.50%) 0 (0.00%) Amoebotania sphenoides 13 (5.00%) 4 (4.44%) 6 (7.50%) 3 (3.33%) TABLE II: Cestod parasite species identified and their corresponding prevalence (%) in traditional backyard chickens (n = 260) from three districts of North Gondar Administrative Zone, Ethiopia. Cestod spp. Age Sex Body condition Adult Grower Males Females Poor Medium Good (n = 208) (n = 52) (n = 123) (n = 137) (n = 33) (n = 85) (n = 142) Raillietina echinobothridia 57 (27.4%) 20 (38.5%) 41 (33.3%) 36 (26.3%) 7 (21.2%) 18 (21.2%) 52 (36.6%) Raillietina tetragona 27 (13.0%) 5 (9.6%) 13 (10.6%) 19 (13.9%) 7 (21.2%) 12 (14.1%) 13 (9.2%) Raillietina cesticillus 3 (1.4%) 0 (0.0%) 1 (0.8%) 2 (1.5%) 1 (3.0%) 2 (2.4%) 0 (0.0%) Choenotaenia infundibulum 7 (3.4%) 3 (5.8%) 4 (3.3%) 6 (4.4%) 1 (3.0%) 5 (5.9%) 4 (2.8%) Hymenolepis cantaniana 22 (10.6%) 4 (7.7%) 8 (6.5%) 18 (13.1%) 2 (6.1%) 10 (11.8%) 14 (9.9%) Hymenolepis carioca 2 (1.0%) 0 (0.0%) 1 (0.8%) 1 (0.8%) 0 (0.0%) 0 (0.0%) 2 (1.4%) Amoebotania sphenoides 10 (4.8%) 3 (5.8%) 8 (6.5%) 5 (3.6%) 2 (6.1%) 3 (3.5%) 8 (5.6%) TABLE III: Cestod parasite prevalences (%) in traditional backyard chickens (n = 260) from three districts of North Gondar Administrative Zone, Ethiopia according to the age, sex and body condition. Nematode spp. Infected (prevalence) Total (n = 260) Wogera (n = 90) Gondar (n = 80) Dembya (n = 90) Ascaridia galli 102 (39.23%) 37 (41.11%) 30 (37.50%) 35 (38.89%) Hetrakis gallinarium 103 (39.62%) 32 (35.56%) 33 (41.25%) 38 (42.22%) Dispharynx nasuta 9 (3.46%) 2 (2.22%) 2 (2.50%) 5 (5.56%) TABLE IV: Nematode parasite species identified and their corresponding prevalence (%) in traditional backyard chickens (n = 260) from three districts of North Gondar Administrative Zone, Ethiopia. Nematode spp. Age Sex Body condition Adult Grower Males Females Poor Medium Good (n = 208) (n = 52) (n = 123) (n = 137) (n = 33) (n = 85) (n = 142) Ascaridia galli 77 (37.0%) 25 (48.1%) 48 (39.0%) 54 (39.4%) 10 (30.3%) 42 (49.4%) 50 (35.2%) Hetrakis gallinarium 83 (39.9%) 20 (38.5%) 48 (39.0%) 55 (40.1%) 15 (45.5%) 43 (50.6%) 45 (31.7%) Dispharynx nasuta 6 (2.9%) 3 (5.8%) 7 (5.7%) 2 (1.5%) 1 (3.0%) 4 (4.7%) 4 (2.8%) TABLE V: Nematode parasite prevalences (%) in traditional backyard chickens (n = 260) from three districts of North Gondar Administrative Zone, Ethiopia according to the age, sex and body condition. Dispharynx nasuta was the least frequently observed nematode (3.46%, found in only 9 cases) (Table IV). Global nematode prevalences and specific prevalences were not significantly affected either by the geographical origin of birds (Table IV), or by the age, the sex and the body condition (Table V). However, the overall nematode infection rate was relatively but not significantly higher in young grower birds (65.38%) than in adults (59.61%) (P > 0.05).

5 366 MOLLA (W.) AND COLLABORATORS Discussion The present study on local backyard chickens in North Gondar Administrative zone, Ethiopia revealed a high prevalence (79.62%) of GIT helminths. The major contributing factor to the high prevalence of these parasitic infections was the type of production system which is basically free-ranging and allows the chickens to scavenge around the house during daytime [16]. The overall helminth prevalence in the current study is comparable with that of YIMER and TEKLE [24] and HAS- SOUNI and BELGHYTI [10] who reported 88.63% prevalence of gastrointestinal helminths in central Ethiopia and 89.9% in Gharb region of Morocco, respectively. However, this finding was lower than prevalences of 97% and 100% reported by SSENYONGA [20] in Uganda and MAGWISHA et al. [12] in Tanzania, respectively. A total of 208 adult birds and 52 young grower birds were considered in the present study and no statistically significant difference in the overall helminth infection rate was observed between the two age groups. Even if the difference was statistically insignificant, young grower birds appeared to be more frequently infected (84.61%) than adults (78.36%) here. In young grower chickens the lowest level of humoral immunity compared to adults [16] may promote susceptibility to helminth infection. Similarly, MUNGUBE et al. [15] also observed a higher prevalence of helminthiasis in younger birds than in adults in Kenya. No significant association between host sex and the frequency of helminth infections was found in the present study that is largely in agreement with previous reports [10], indicating that there is no usually a natural affinity of helminth species to either sex of the host bird. The recording of multiple helminth infections in the current study suggests that the prevailing environmental conditions and free- range management systems were favourable for simultaneous development of the different poultry helminth parasites. The recording of multiple infections with helminth parasites was reported in other different studies conducted on backyard poultry [3, 6, 15, 18]. As far as cestod infections were concerned, different cestod species were identified in the gastrointestinal tract from 142 (54.62%) chicks. Seven species of tapeworms were observed. The most prevalent cestod recorded in the North Gondar Administrative zone was Raillietina echinobothridia (29.62%). The observed result in the current study is comparable with reports of ASHENAFI and ESHETU [1] in central Ethiopia and MUNGUBE et al. [15] in Eastern Kenya. However, this prevalence is slightly lower than previous ones reported from different parts of the country, 45.69% in 4 districts of Amhara region [6], 36.95% in and around Soddo [22] and 52.75% in and around Dire Dawa [3]. Another study conducted by PHIRI et al. [18] in free- range chickens in central Zambia indicated a markedly higher prevalence (81.6%) for the same parasite. However, the occurrence of this parasite even with a lower prevalence than previously reported is economically important [13]. The corresponding prevalences of R. cesticillus and R. tetragona in the present work was low compared to the observations of ASHENAFI and ESHETU [1] in central Ethiopia, ESHETU et al. [6] in Eastern Amhara (North Eastern Ethiopia), GEDION [7] and BERSABEH [3] in Eastern Ethiopia. This prevalence is also low compared to reports in other African countries [15, 17]. This might be due to less availability of the intermediate hosts such as dung beetles, ants etc. of these parasites. Davainea proglottina, the most pathogen cestod species of poultry, was not recorded in this study. Prevalence rates of 19.4% in semi-arid zones of Eastern Kenya [15] and 1.12% in Amhara region [6] were previously reported, but in agreement with the present study ASHENAFI and ES- HETU [1] did not record this parasite in their study in central Ethiopia. In the present study, a statistically significant difference (P < 0.05) was observed in the cestod prevalence among the three selected districts; higher infection rates were observed in chickens from Gondar town and Dembya (representing midland regions) than in the Wogera district (representing highland regions). This indicates that the difference in the agro-ecology influences the life cycles of cestodes, which might be explained by the presence of favourable microenvironment for the survival of intermediate hosts and transmission of the parasite in midland areas [1]. At higher altitudes, low temperatures of the highland areas may inhibit the development and survival of early infective larval stages and hence limit the access to intermediate hosts and later to final hosts, leading to lower infestation rates. This is supported by Mc DOUGALD and REID [13], who stated that tapeworms are found more frequently in warmer areas where the intermediate hosts are abundant than in colder areas. In the present study three nematode parasites, namely Hetrakis gallinarium, Ascaridia galli and Dispharynx nasuta were identified from different segments of gastrointestinal tracts of examined birds. The most prevalent nematode specie encountered was Hetrakis gallinarium (39.62%) which was comparable to prevalences of 43.24% and 32.61% respectively established by BERSABEH [3], and ASHENAFI and ES- HETU [1] in central Ethiopia. ESHETU et al. [6] reported a lower prevalence (17.28%) in Eastern Amhara region to the same parasite. Another study in semi-arid zones of Eastern Kenya indicated a prevalence of 22.8% [15]. Ascaridia galli was the second most prevalent (39.23%) nematode identified in this study. This finding is comparable with 33.3% prevalence determined in Kenya [15] and 29% found in adult chickens of Tanzania [12]. Nevertheless, previous studies in southern Ethiopia [22] and central Ethiopia [1] reported higher prevalences, 64.3% and 55.3%, respectively. Wet and humid conditions are necessary for the development of Ascaridia galli eggs to infective stages and the rise of earth worm population that serves as a paratenic host for this parasite [15, 16]. However, this study was undertaken in a dry season of the area and this might be the reason for low occurrence of the parasite in the study area. Other nematode parasite identified in the present study was Dispharynx nasuta which occurred at a prevalence of 3.46%. This is the least frequently occurring parasite recorded and its prevalence is in general comparable with the reports of MAGWISHA et al. [12] and ASHENAFI and ESHETU [1]. HASSOUNI and BELGHYTI [10] reported prevalence of 5.3% in backyard poultry of Morocco. Heavy infestation by D. nasuta interferes with enzymatic digestion because of nodules formed on the mucosa of proventriculus [15].

6 GASTRO-INTESTINAL HELMINTHS IN CHICKENS FROM NORTH GONDAR 367 The occurrence of these parasites was not linked significantly to any of risk factors (age, sex, body condition, and agro-ecology) considered during the study period. Lack of significant association with respect to sex and body condition was also reported by some authors for poultry nematodes [6, 15]. As a conclusion, the present study clearly indicated that local chickens kept under traditional or backyard system in the study area were highly infested and exposed to wide variety of gastro-intestinal helminth parasites. The damage inflicted by such highly prevalent gastro-intestinal helminth infection in view of the economic importance of the rural poultry production, in the study area particularly and in the country generally will undoubtedly be high. It is therefore, recommended that integrated control strategies have to be put in place since there is little effort directed currently towards this problem. 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