Livestock Research for Rural Development 27 (6) 2015 Guide for preparation of papers LRRD Newsletter

Citation of this paper

Gastrointestinal-parasites infestation in Yankasa sheep in a semi-arid environment

N K Alade and M D Bwala

Department of Animal Science, Faculty of Agriculture University of Maiduguri
P. M. B 1069, Maiduguri, Borno State, Nigeria


This study was conducted in Maiduguri, Nigeria to determine how Gastrointestinal parasites infestation were affected by sex, season, age and body weight and their relationship with haemoglobin concentration in Yankasa sheep. A total of 135 faecal and 135 blood samples were collected in each of the two seasons (dry and raining) of the year 2014, from University of Maiduguri Livestock teaching and Research Farm, University of Maiduguri Veterinary Large Animal Clinic and the Maiduguri Abattoir. The feacal samples were analysed for gastrointestinal parasite eggs and Haemoglobin concentration of the blood sample were analysed. The gastrointestinal parasites egg count was estimated using the Modified Mcmaster technique and the haemoglobin concentration was determined using cyanmethaemoglobin method.

Five species of gastrointestinal parasites eggs discovered were; Strongyle, Strongloides, Coccidian occyst, Moniezia, and Trichuris with mean counts of 1080, 320, 1208, 30.2 and 1.60, respectively. There were significant differences (P<0.05) between the mean gastrointestinal parasites egg counts among animals of different sexes, age groups, body weight groups, blood haemoglobin concentrations and in different seasons of the year. Females (3631/ 67.3 %) had higher overall mean parasites egg counts and prevalence than the males (1747/ 53.4%), the raining season (2959/ 67.4 %) was higher than the dry season (2559/ 53.3 %). Age wise, suckling animals (3286 / 68.3 %) were more infected than the young (2999/ 59.3 %) and adult (1993/ 53.5 %). The group06-31 kg had the highest overall mean egg count and prevalence (3151 / 68.8 %) than the other groups 32-57 kg (1812/ 62.4 %) and 58-81 kg (1125 / 49.7 %). The group with haemoglobin concentration of 5.7-8.3 g/dl had the highest overall mean parasitic egg counts of 3468 (67.9 %) than those of the groups of 8.4-11.3 g/dl and 11.4-14.3 g/dl having 2837 (59.5 %) and 1988 (53.7 %), respectively; an indication that blood haemoglobin concentration and parasites egg counts were negatively correlated.

Key words: haemoglobin concentration, Nigeria, prevalence, resistance


Despite the remarkable achievement in the discovery of gastrointestinal parasites drugs with ever increasing spectra of activity, nematode parasitic infestation and disease remains one of the greatest limiting factors in the production of sheep worldwide (Perry and Randolph 1999). The effects of gastro intestinal nematode pose a serious limitation to small ruminants due to associated morbidity, mortality, cost of treatment and control measures (Nwosu et al 2007). Coop and Holmes (1996) reported that gastrointestinal helminthes are major contributors to reduced productivity and can lower the production of meat, milk and wool. Also the gastrointestinal nematode infestation resulted in negative influence on both the average daily gain of body and the rate of growth of wool (Niezen et al1995). Gastrointestinal nematodes are an important problem in sheep and are responsible for heavy loses especially in tropical and subtropical areas, like Nigeria (Mendoza et al1998).

The major factor that influences gastrointestinal parasites infestation in small ruminants, especially sheep is exposure to faecal contamination of grazing land (Pathak, 2011). Pathak and Pal (2008) reported that poorly nourished animals maintained on poor quality roughage which are deficient in protein, energy, minerals and vitamins are also susceptible to parasitic infestation. Greer (2008) maintained that the degree of nematode infestation varies according to the host immune response to these worms. Other factors are sex, age, body weight and season. Males are generally known to be more susceptible to gastrointestinal nematode infestation than females due to the production of androgen hormone which lowers immune response in males (Asif et al2008). Regarding age of the host animal, higher infestation of suckling than young and adult animals may be attributed to a weaker immunological response of young animals. Authors like Tariq et al (2010) and Zeryehun (2012) reported that older animals also recover from parasitic infection more quickly as the immunity of the host increases with age; due to repeated exposure (Dagnachew et al 2011). The body weight of animals has been known to affect infestation of gastrointestinal nematodes, as heavier animals show more resistance to gastrointestinal nematode infestation due to sufficient body fat reserves that aids in increasing immune response of the animal (Bilbo and Nelson2001). During rainfall the number of infective larval stage of nematodes are increased, thereby making the animal more susceptible to infestation whereas the infestation is generally less during the dry season (Kantzoura et al2012).

Traditional control of worms which heavily depends on anthhelmintic intervention within the host may be broadly categorized as suppressive, strategic, tactical or curative. Suppressive control involves administration of anthelmintics before clinical signs of gastrointestinal nematodes are expressed there by suppressing the population of gastrointestinal nematodes in the host. Strategic control of gastrointestinal nematodes is an integrated approach, where anthelmintics are combined with management to reduce gastrointestinal nematodes infestation (Badran et al 2012). Tactical control is based on routine monitoring of environmental or parasite associated variables and intervention with anthhelmintic when threshold values are reached (Walkden-brown and Eady 2003). Curative control on the other hand involves administration of anthelmintics after clinical signs of gastrointestinal nematodes infestation are observed. Curative treatment is uneconomical because of the loss of production that occurs before treatment (Besier and Love, 2003).

Due to the resistance to anthelmintics, a global search for alternative and more sustainable solution to gastrointestinal nematodes infestation is needed (Kaplan 2004). Gasbarre and Miller (2000) reported that, though replacement of a susceptible breed with a resistant breed is one method of genetically improving resistance to nematode parasites, selection for resistant animals within a breed is also viable. The measurement of antibody levels in blood is used to assess the level of resistance to gastrointestinal nematode infestation and serves as a basis for selection (Kemper et al2010). Haemoglobin polymorphism is also known to vary with resistance to gastrointestinal nematodes. Hence it could be a yardstick for selection against nematode infestion. For example haemoglobin A (HbAA) has higher resistance to helminth (FAO 1988; Herselman et al (2006). This resistance was attributed to its higher affinity for oxygen and haemoglobin concentration (Di Stasio 1997).

This work is aimed at studying gastrointestinal parasites infestation as affected by age, body weight, sex and season and also determines its relationship with haemoglobin concentration in Yankasa sheep.

Materials and methods

Study area

The study was carried out in Maiduguri, Borno state. Maiduguri, the Borno State capital is situated on latitude 1105’N, longitude 13009’E (Encarta 2007) and at an altitude of 354m above sea level. The area falls within the Sahelian region of West Africa, which is noted for great climatic and seasonal variations. It has very short period (3–4months) of rainfall of 645.9 mm/annum with a long dry season of about 8–9 months. The ambient temperature could be as low as 200C during the dry cold season and as high as 440C in the dry hot season. Relative humidity is 45% in August which usually lowers to about 5% in December and January. Day length varies from 11 to 12hours (Alaku 1982).

Sample collection

A total of 270 blood and 270 faecal samples were collected from Yankasa sheep in two seasons (dry and raining seasons). In each of the two seasons 135 blood and 135 faecal samples were collected from University of Maiduguri Livestock Teaching and Research Farm, University of Maiduguri Veterinary Large Animal Clinic and the Maiduguri Abattoir. The animals were kept under a semi-intensive system with minimal grazing and supplemental feeding with preserved hay and concentrates. The animals were ear tagged for identification, vaccinated against common diseases and dewormed twice a year with Ivermectin (Ivomec® Liquid and Primectin™ drench) at the onset of raining and dry seasons. The herd consisted of adult sheep (>3years), young (1-2 years) and suckling lambs (<1 year) and their body weight ranges from 06 kg to 81 kg. The animals used for the study were classified by age (suckling, young and adult) as described by Raza et al (2014), weight (06-31 kg, 32-57 kg and 58-81 kg) and sex.

Blood sample collection

Blood samples (5 ml per animal) were obtained from the jugular vein and placed in tubes with EDTA (Ethylene-diamine tetra-acetic acid) as anticoagulant. The samples were labelled appropriately. The haemoglobin concentration was determined using cyanmethaemoglobin method (Addas et al 2010).

Faecal sample collection

Fresh faecal sample was collected directly from the rectum of the animal (approximately 5g) through rectal stimulation by fingers. The faecal samples were placed in universal containers with appropriate labels. Samples which were not examined within 24hours were stored with 10% formalin and examined the next day.

The faecal samples were processed for quantative examination of gastrointestinal parasites. Samples found positive for gastrointestinal parasites were subjected to Egg per gram (EPG) counting using the modified Mcmaster technique following standard procedures as described by Soulsby (1986). The floatation solution used was NaCl. The identification of the eggs was made on the basis of their morphology. The mean egg count was arrived at after taking the average of three counting intervals.

Statistical analysis

Data collected was analysed using the General Linear Model procedure of SPSS 20.0 with season, age, sex, body weight and blood haemoglobin concentration as fixed factors. Significant, means were separated by Duncans’ Multiple Range Test. The overall means and prevalence were calculated using descriptive statistics. The statistical model used for the analysis is as follows

Yijklm = µ + Ai + Bj+Ck + Dl + Fm+ eijklm

Where; Yijklm = Individual gastrointestinal parasites egg species count,

µ = General mean,

Ai = Effect of season

Bj= Effect of age,

Ck = Effect of sex,

Dl = Effect of body weight,

Fm= Effect of blood haemoglobin concentration

eijklm = Random residual error.

Results and discussion

Quantitative gastrointestinal parasites egg count

Mean gastrointestinal parasites egg counts (an average of three counting intervals) in relation to season, age, sex, body weight and haemoglobin concentration are presented on Table 1. The overall mean egg count for the study was 2759 with a prevalence of 60.4 %. This result is in concordance with that of Solomon-Wisdom et al (2014) where they discover a prevalence of 68.80 %. This finding is lower when compared to the studies of Moti (2008), Tefera et al (2011) and Ayele et al (2014) who reported overall prevalence of 79.1 %, 91.3 % and 76.3 %, respectively. The higher prevalence recorded by these authors could be ascribed to differences in management, nutrition and frequent exposure to communal grazing pasture that have been contaminated.

Five species of gastrointestinal parasites found were Strongyle, Strongloides, Coccidianoocyst, Moniezia, and Trichuris with mean egg counts of 1080, 320, 1208, 30.2 and 1.60, respectively. Faizala and Rajapakse (2001) reported that Coccidia and other gastrointestinal nematodes as mixed or single infections are the major parasitic diseases of sheep and goats in tropical and temperate climates. The results disagree with the findings of Regassa et al (2006) and Temesegen (2008) who reported prevalence rates of 70.2% and 66.6%, of stronglye in studies conducted in different regions of Ethopia. However, Lateef et al (2005), Asif et al (2008) and Hamdullah et al (2013) recorded infection as high as 28.8% for Trichuris. The disparities in the levels of infestation might be due to differences in ecology, temperature and pasture management.

Effect of season on gastrointestinal parasites egg count

The mean parasitic egg counts of 1202 (Strongyle) and 56.3 (Moniezia) during the dry season were significantly (P<0.05) higher than the corresponding values of 852 and 0.00 recorded for raining season. (Table1.) On the other hand, Strongloides, and Coccidian oocyst species had significantly (P<0.05) higher mean parasites egg counts in the raining season (384 and 1402) than dry season (256and 1014). The overall mean parasitic egg counts of 2959 and prevalence of 67.4 % in the raining season were higher than the dry season (1747.20 and 53.4 %). This result is in agreement with those of Bashir et al (2012) who reported a prevalence rate of 48.2% and 32.5% for raining and dry seasons respectively and Lemma and Abera (2013) who reported corresponding values of 88.2% and 51.5%. Higher prevalence of gastrointestinal parasites egg counts in the raining season might not be unconnected with favorable climatic condition that encourages survival of worms.

High rainfall in spring also helps in providing suitable molarities of salt present in soil which is an important factor for ecdysis (Soulby, 1986). Usually larvae of important gastrointestinal parasites are able to undergo a period of arrested development (hypobiosis) in host following infections when conditions in the external environment are least favourable for development and survival of eggs and larva. This suspension of development helps some parasites to survive the dry seasons (Michael et al 1975).

In contrast to these findings, Nabavi et al (2011) discovered that, in sheep, there was no correlation between the prevalence of gastrointestinal parasites in sheep and seasons. This is an indication that species of gastrointestinal parasites thrive equally in all seasons and may be due adequate management and treatment of the animals on the part of the owners. Moreover, limitation in grazing pastures due to rise in price of land can decrease the available pastures which can then be substituted with hand feeding and, hence, less worm infections.

Effect of sex on gastrointestinal parasites egg count

Females generally had significantly (P<0.05) higher mean egg counts of Strongyle,(1202), Coccidian oocyst (1915) andMoniezia (47.2) than the males which had higher mean egg counts of 958, 501 and 13.3 for Strongyle, Coccidian oocyst, and Moniezia respectively. The males had significantly (P<0.05) higher mean egg counts for Trichuris (2.44) than the females (0.77). The overall mean egg counts and prevalence were higher in the females (3631 and 67.3%) than the males (1747 and 53.4%). The result agrees with the studies of several authors where females were observed to be generally more infested than the males. Al-shaibani et al (2008) found of prevalence rate of 68.3 % and 44.4 % in females and males, respectively. Bashir et al(2011) discovered the infestation rate in females and males to be 57.2% and 42.8% respectively, Hamdullah et al(2013) found the prevalence of 56.9% and 42.1% among females and males respectively and Raza et al(2014) who also discovered infection rate to be higher in females (82.6%) than the males (66.4%). The higher prevalence in females may be attributed to reproductive physiological stress during pregnancy and parturition which lower their resistance and also due to their enhanced grazing during lactation.

This result is however in contrast to the findings of Regassa et al (2006), Qamar (2009), Lemma and Abera(2013) and Ayele et al (2014), who discovered that both sexes were equally infected and this was attributed to equal exposure of both sexes to the same grazing pasture and being from similar agro-ecology. Another contrasting view was expressed by Mushtaq and Tasawar (2011) who stated that males had significantly higher gastrointestinal parasites egg counts than females. Bilbo and Nelson (2001) reported that such differential prevalence of gastrointestinal nematodes in sheep may be due to stimulatory effects of estrogens on immune responses in females, whereas androgen has an opposite effect in males (Urquhart et al 1996). The higher prevalence in the males could also be due to better management and treatment of the female animals during pregnancy and lactation.

Table 1: Mean gastrointestinal parasites egg count in relation to season, sex, age, body weight and haemoglobin concentration.




Coccidian oocyst



Overall mean















56.3±53.0 a

2.41±2.83 a


53.3 %






0.80±2.67 b


67.4 %



958±652 b



13.3±52.3 b

2.44±2.79 a


53.4 %


1202±631 a

322±239 a


47.2±50.7 a

0.77±2.70 b


67.3 %




489±297 a


42.4±63.3 a

1.79±3.37 a


68.3 %



205±282.5 b


27.5±60.0 b

1.63±3.20 a





267±215 b


20.7±45.6 b

1.63±2.43 a



Body weight

06-31 kg

1171±280 a



44.9±22.5 a

0.89±1.20 a


68.8 %

32-57 kg

832±487 b

271±184 a


15.7±39.1 c

3.67±2.09 a


62.4 %

58-81 kg

1237±1635 a

326±619 a


30.0±31.3 b

0.24±7.01 a


49.7 %

Haemoglobin concentration




927±154 b

19.0±62.0 b






387±233 a

1985±1234 a

50.4±49.5 a



59.5 %



328±257 a

1012±1361 b

21.3±54.6 b



53.7 %

Values in columns within subsets with different superscripts are different from each other (P<0.05).

Effect of age on gastrointestinal parasites egg count

The mean parasitic egg counts was significantly (P<0.05) higher in the suckling animals for Strongloides, Coccidian oocyst and Moniezia followed by the young animals then the adult had the least. The suckling animals had the following mean parasitic egg counts; 670, 489, 1527 and 42.4 for Strongyle, Strongloides, Coccidian oocyst and Moniezia respectively, the young had 1845, 205, 1275 and 27.5 forStrongyle, Strongloides, Coccidian oocyst and Moniezia respectively and that of the adult animals were; 742, 267, 822 and 20.7 for Strongyle, Strongloides, Coccidian oocystand Moniezia respectively. The overall mean parasites egg counts and prevalence were 3286(68.3 %), in the suckling. Corresponding values for young and adults were 2999 (59.3 %) and 1993(53.5 %).

This result is in agreement with the study of Al-Shaibani et al (2008) who reported prevalence of 53.6 %, 50.6 % and 28.7 % for lamb, young and adult respectively in sheep. Similarly, Lemma and Abera (2013) reported 79.6 % (lambs), 70.4 % (young) and 62.4 % (adult). Raza et al (2014) also make a similar observation. Young animals are more susceptible to worm infestation due their weaker immunological response. This can be linked to weaning stress, low live weight and fat reserves or inadequate nutrition. Zeryehun (2012) reported that older animals recover from parasitic infection more quickly as the immunity of the host increases with age. The adults might have also acquired immunity due to frequent exposure and there is tendency for them to expel the ingested parasites eggs infection.

In contrast to these findings, Tasawar et al (2011) reported higher prevalence in older animals than the younger ones and attributed this to the fact that the younger animals graze less contaminated pastures and are mostly fed with supplemental feed. Adult sheep, on the other hand graze on larger area of pastures being contaminated with various flocks and are subjected to different stress conditions like climate, long daily movement and gestation. Abunna et al (2007), Bikila et al (2013) and Ayele et al (2014) discovered that there was no difference in the prevalence between age groups and attributed this to equal exposure of the animals to the same grazing pastures and that even if the lambs graze less contaminated pasture, they might get infected from contaminated pasture being spread for the dams. Ayele et al (2014) ascribed the insignificant effect of age on parasites infestation to the small number of young animals in their research.

Effect of bodyweight on gastrointestinal parasites egg count

The mean parasitic egg counts for the weight group of 6-31 kg were 1171, 1846 and 44.9 for Strongyles, Coccidian oocyst and Moniezia respectively which were significantly (P<0.05) higher than those of the weight group of 32-57 kg with mean parasites egg counts of 832, 1377 and 15.7 for Strongyle, Coccidian oocyst and Moniezia respectively and those of the weight group of 58-81 kg was 1237, 401 and 44.9 for Strongyle, Coccidian oocyst and Moniezia respectively. The group with the lighter weight (6-31 kg) had the highest overall mean parasitic egg counts (3151) and prevalence of (68.8 %) which were higher than the corresponding values of 1812and (62.4 %) for weight group of 32-57 kg and 1125 and (49.7%) for weight group of 58-81 kg.

This result is in consonance with the findings of Lemma and Abera (2013) where animals with poor body condition had the highest prevalence of 81.3 %, compared with 69.5 % and 61.5 % for those with medium and good body conditions respectively. Bashir et al (2012), Hamdullah et al (2013), Diriba and Birhanu (2013) and Ayele et al (2014) reported similar findings. The high prevalence in the animals with poor body condition can be attributed to the fact that well fed animals develop good immunity that suppresses the fecundity of the parasites. Tasawar et al (2011) stressed that lack of sufficient fat reserves, poor health and nutritional factors may be the primary reasons why light animals are less able to mount protective immunity against worm infestation.

Relationship between Haemoglobin Concentration and Gastrointestinal Parasites Egg Count.

The overall mean parasitic egg counts and prevalence showed that the lowest haemoglobin concentration group (5.7-8.3 g/dl) had higher parasitic egg counts and prevalence than the other two groups (8.4-11.3g/dl and 11.4-14.3g/dl). This is in agreement with the findings of Fantu et al (2012) who reported that faecal egg count was negatively correlated with haemoglobin concentration and Kasali et al (1988) that indicated low PCV and high EPG levels in nematode infected animals. This shows that blood haemoglobin concentration and parasitic egg counts are negatively correlated and, it can therefore be concluded that the level of parasites had negative effect on blood haemoglobin concentration.



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Received 5 February 2015; Accepted 10 April 2015; Published 3 June 2015

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