Prevalence of Eimeria species of the domestic goats Capra hircus Linnaeus , 1758 in Al-Baha area , Saudi Arabia

This work aimed to identify Eimeria species of goats and to investigate the factors that might potentially influence their prevalence and parasite load. This study was conducted in Al-Baha area, south-west Saudi Arabia from September 2011 to June 2012. Out of 336 faecal samples examined, 180 (53.57%) were positive for Eimeria oocysts. The prevalence of Eimeria ranged from 39.64% to 61.40% in different localities. Nine different Eimeria species were identified from faecal samples of goats. Eimeria species were: Eimeria arloingi (35.71%), E. alijevi (26.19%), E. hirci (25.29%), E. ninakohlyakimovae (16.36%), E. christenseni (14.59%), E. caprina (11.31%), E. jolchijevi (9.52%), E. caprovina (5.59%) and E. apsheronica (3.27%). E. arloingi (35.71%), E. alijevi (26.19%) and E. hirci (25.29%) were the most prevalent species and E. apsheronica (3.27%) was the least prevalent one. The main factors affecting prevalence and parasite load of Eimeria species were host age, locality and season. Significant negative correlations were found between host age and both prevalence and OPG number. Multiple-species infections were detected in 89.44% of positive goats which carried two to five species. In conclusion, the prevalence of coccidiosis is relatively low compared to other studies. Moreover, no signs of clinical coccidiosis were found in this study. We need further research to study the interaction between multiple-species infections in coccidiosis and parasite load in natural host-parasite systems.


INTRODUCTION
Domesticated small ruminants, especially goats, constitute an important source of animal protein to most inhabitants in Saudi Arabia.A lot of socio-economic importance is therefore attached to ownership of these animals.However, the productivity of goats is constrained by parasitic infections (Dhar et al., 1982;Ibrahim et al., 2008).Coccidiosis is a worldwide distributed disease and one of the most economically important infections that threatening goats production (Alyousif et al., 1992;Gül, 2007;Wang et al., 2010;Cavalcante et al., 2012).Coccidiosis is a parasitic disease caused by intracellular protozoa called Eimeria.Eimeria can invade and destroy intestinal cells of the hosts, causing anaemia, electrolyte loss and poor absorption of nutrients.The most common sign of infection is diarrhoea, and affected goats can show a rough hair coat, poor weight gain and weakness (Wang et al., 2010).
Thirteen Eimeria species have been reported from the goats (Pellérdy, 1974;Levine, 1985;Norton, 1986;Wang et al., 2010).In Saudi Arabia, ten Eimeria species have been found in goats, namely E. arloingi, E. alijevi, E. ninakohlyakimovae, E. hirei, E. christenseni, E. caprina, E. apsheronica, E. caprovina, E. punctate and E. jolehijevi (Alyousif et al., 1992).Alyousif et al. (1992) showed that infection of goats with Eimeria species is common in the central region of Saudi Arabia.There are no studies of prevalence of Eimeria infection in goats in Al-Baha area, which has unique climatic and geographic conditions different from other areas of Saudi Arabia.This area has very cold and dry winter season, but has a warm and rainy temperate climate during the spring and summer seasons in Al-Baha locality.Therefore, the objective of the present study was to investigate the factors affecting in prevalence and parasite load of Eimeria species of goats.The results obtained would be quite useful to devise appropriate and effective control strategies and prophylactic programs for coccidiosis of goat unique to this climatic zone and other parts of the world with similar climatic and husbandry production systems.

The study area
The study was conducted in Al-Baha area, south-west Saudi Arabia (20°N, 41-42°E) from September 2011 to June 2012.The study area is mainly hilly, with small areas of either mountainous or flat land and extends from 500 to 2500 m a.s.l.The climate in Al-Baha has two extremes.Mild winters and hot summers, with an average annual rainfall between 100 and 250 mm, prevail in the lowlands; cold winters and mild summers, with an average annual rainfall between 229 and 581 mm, prevail in the highlands (Ibrahim et al., 2008).

Sample collection
A total of 336 goats from three localities in Al-Baha area were randomly chosen from each sheepfold.Faecal samples of approximately 3-5 g were collected directly from the rectum using examination gloves.All samples were placed into plastic bags and were classified into three age categories: < 6-months old (90 goats), 6-12-months old (121 goats) and >12-months old (125 goats) and two seasons (dry: September 2011-January 2012 and wet season: February 2012-June 2012).The structure of the sampled host population of goats according to season, locality, sex and age categories was shown in Table (1).The collected samples were stored at 4°C until being examined.

Sample processing and recovery of Eimerian oocysts
Faecal samples was examined for the presence or absence of eimerian oocysts by a flotation technique using saturated saline.Oocysts per gram of faeces (OPG) were quantified using a modification of the McMaster technique (MAFF, 1986).
Oocysts in two chambers of the McMaster slide were counted and the sum number of oocysts in both chambers was multiplied by the dilution factor (100) to obtain an estimation of the number of OPG of each faecal sample.Each faecal sample was examined three times using the same method (Wang et al., 2010, Cavalcante et al., 2012).The results are expressed as the mean value of the three independent examinations.

Eimerian species identification
After examination, positive samples were filtered through sieves covered with folded gauze and centrifuged at 250 × g for 10 min.Filtered material was placed into Petri dishes with 2.5% potassium dichromate solution (K 2 Cr 2 O 7 ) for sporulation at laboratory temperature.After sporulation, sporulated oocysts were recovered by centrifugation in saturated saline solution at 250 × g for 5 min followed by washing with distilled water.Concentration of sporulated oocysts was performed by centrifugation at 250 × g for 10 min, stored in potassium dichromate solution at 4°C for subsequent study.The oocysts were identified based on their morphological characteristics (size, shape, colour, form index, presence or absence of micropyle and its cap, presence or absence of residual, polar and stieda bodies) of the oocysts and sporocysts (Pellérdy, 1974;Levine, 1985;Soulsby, 1986;Wang et al., 2010;Cavalcante et al., 2012).To ensure that species identification is valid, when possible, at least 50 sporulated oocysts from each species were observed and measured (Wang et al., 2010, Cavalcante et al., 2012).

Data analysis
Prevalence was calculated according to Bush et al. (1997).Differences in prevalence of Eimeria among different age categories of goats, as well as among different localities were evaluated using a Chi square test.Comparisons of OPG numbers according to sex and season were tested using Mann-Whitney test (U-test) while according age categories and locality were tested by Kruskal Wallis.Correlations between host age and both prevalence and OPG number were examined by using the non-parametric, Spearman's rank correlation coefficients (r s ).All the statistical tests were performed by using the software packages SPSS 17.0 (USA) and a value of P < 0.05 was considered significant.
There was seasonal difference in prevalence of Eimeria oocysts in goats.The prevalence of coccidial oocysts was significantly higher (60.22%) in wet season than that in dry season (45.81%) (Χ 2 =9.81, df=1, P=0.008).OPG numbers were significantly higher (173.15±27.56)when compared to that in dry season (Table 6; U=12366.5, P=0.049).Multiple-species infections (simultaneous infections with multiple parasite species in an individual host) of more than one Eimeria species were commonly present in all age categories.Multiple-species infections were detected in 89.44% (161/180) of positive goats which carried two to five species; 67.77% (122/180) of positive goats had two to three species.Infections with 4 and 5 species were less common (21.66%; 39/180) (Table 7).

DISCUSSION
In the present study, the prevalence of Eimeria species infection was 53.57% in goats in Al-Baha area, south-west Saudi Arabia.This finding is lower than those reported in central region of Saudi Arabia (Alyousif et al., 1992), Turkey (Gül, 2007), northeastern China (Wang et al., 2010), Barazil (Cavalcante et al., 2012), which revealed a prevalence of 90.3%, 82.55%, 90.9%, 91.2% in goats respectively.These differences in prevalence may be due to various sanitation efforts in the management programs attempted by goat producers to control coccidiosis or due to differences in ecological condition.
The prevalence and OPG of Eimeria oocysts in lower age category (kids) (89.5%) were significantly higher than that in adult goats (87.5%).Moreover, the number of Eimeria oocysts excreted in the group less than 1-year-old group was higher than older (>1-year-old) animals investigated.These findings are in agreement with previous observations (Alyousif et al., 1992;Wang et al., 2010).This has been attributed to lower resistance or less immunity to Eimeria species in young animals compared to the older animals (Gregory et al., 1980;Kanyari, 1988;Maingi and Munyua, 1994).
In the present study, the prevalence and OPG of Eimeria species in wet season (60.22% and 173.15±27.56OPG respectively) were significantly higher than that in dry season (45.81% and 134.60±24.00OPG respectively).Similarly, Bakunzi et al. (2010), El-Bahy et al. (2008) and Majaro and Dipeolu (1981) found higher Eimeria oocyst counts during the hot, rainy season than those during the cold, dry season.El-Bahy et al. (2008) reported that Coccidia sp. are abundant during April to June and their incubation period is about 1-2 week, so new infection could be occurs in the same period as end of March till end of June.On the contrast, other researchers observed that the overall OPG counts of goats were significantly higher during the dry season than those during the wet season (Harper and Penzhorn, 1999;Soliman and Zalat, 2003).
In conclusion, the prevalence of coccidiosis is relatively low compared to other studies.Moreover, no signs of clinical coccidiosis were found in this study.We need further research to study the interaction between multiple-species infections in coccidiosis and parasite load in natural host-parasite systems.These results also provide relevant base-line data for assessing the effectiveness of future control strategies against coccidiosis in goats.

Table 3 :
Prevalence of Eimeria species in goats.

Table 4 :
Prevalence and parasite load of Eimeria oocysts per host sex of goats.

Table 5 :
Prevalence and parasite load of Eimeria oocysts in different age categories of goats.

Table 6 :
Prevalence and parasite load of Eimeria oocysts in different seasons in Al-Baha area, Saudi Arabia.

Table 7 :
Percentage of single and multiple-species infections of different Eimeria species in goats in Al-Baha, Saudi Arabia.