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Coproscopic Study on Enteric Protozoan Parasites of Goats (Capra hircus L., 1758) in Upper Egypt.

Byline: Ismail Saad El-Shahawy

Abstract

The present study was described the occurrence of various enteric protozoan parasites of goats in Upper Egypt region. Coprological examinations were performed in assessment. A total of 252 goats were scanned for their intestinal coccidian parasites. Out of these 164 (65.07%) were oocyst of Eimeria spp. and 17(6.74%) Cryptosporidium species detected in goats, respectively. Additionally, Statistically significant variation (P =0.002) was observed in the prevalence rate of Eimeria infection among different age groups, while there was no significant seasonal variation observed in studied animals. Seven Eimeria species were identified in fecal samples namely; Eimeria alijevi (50%), E. arloingi (46%), E. caprovina (38%), E. ninakohlyakimovae (20%), E. hirci (18%), E. jolchijevi (12%) and E. aspheronica (10%).

Furthermore, the most prevalent species in kids was found E. arloingi, while E. alijevi in adult goats. The number of oocysts excreted were found lower (1200 OPG) in adult goats , as compared to kids (3400OPG). The present study indicates that coprological survey was considered as good tools for demonstrating the most prevailing parasites of the examined region, and subsequently for appropriate control approach.

Key words: Cryptosporidium; Egypt; Eimeria Endoparasite; Goats; Prevalence

INTRODUCTION

The domestic goat (Capra hircus L., 1758) is phylogenetically more adapted to unfavorable conditions having ability to efficiently convert low-quality vegetable matter into energy-dense fat, muscle, and milk (Oltjen and Beckett, 1996). Additionally, the world population and its demand for food are growing rapidly so rearing small ruminants has become more interesting in recent years. Management, nutritional and sanitary problems still plague the livestock business despite good production indicators (Cavalcante et al., 2012).

Caprine coccidiosis caused by the apicomplexan protozoan genus Eimeria is a worldwide and frequent intestinal parasitosis of goats (Agyei et al., 2004). It affects the profitability of the industry, particularly in rural, semi-arid geographic regions that are economically dependent on goat rearing, such as the Mediterranean basin (Ruiz et al., 2006), Africa (Kanyari, 1993), Asia (Faizal and Rajapkse, 2001) and Latin America (Cavlcante et al., 2012). Moreover, it is one of the most pathogenic infections responsible for considerable morbidity and mortality particularly in young kids. Profuse diarrhoea, loss of body weight, reduction in milk yield, nervous symptoms and death have been the effects in this infection (Pellerdy, 1974).

Cryptosporidiosis is a prevalent disease in neonatal ruminants and humans. It is caused by Cryptosporidium parvum, which is primarily the disease of lambs and kids <30 days of age, and is usually a milder disease than coccidiosis (Fischer, 1984). Likewise, Cryptosporidium infection of livestock may have an important economic impact on farmers because of high morbidity and sometimes high rates of mortalities, the excreted Cryptosporidium oocyst with feces of infected animals, particularly kids can be considered as a source of human infection.

Therefore, knowledge of prevalence of enteric protozoan parasites and current species will help to minimize the economic losses in the goat industry, evaluate infection potential and control programs, especially for kids. Hence, the present research was designed to determine the epidemiological features of these parasites among our native goats at Upper Egypt area, Egypt.

MATERIALS AND METHODS

Study area

The study was conducted on goats of Qena region, Upper Egypt. Qena, the origin of the study animals, which lies between 26deg10'12"North and 32deg43'38"East in the south part of Egypt. Qena region has a hot desert climate, with very hot summers and very little precipitation year round.

Study animals and sample collection

In a cross-sectional study from January 2014 to January 2015, 252 faecal samples were collected randomly from goats of different age and sex. None of the animals showed clinical signs of disease. Faecal samples were collected directly from the rectum of each animal using disposable examination gloves. The samples were collected into plastic bags, labelled and analyzed using standard coprological techniques at the laboratory of Parasitology Department - Faculty of Veterinary Medicine- South Valley University, Egypt (Pavlovic et al., 2010).

Parasitological examination and species identification of coccidian oocysts

The coccidial infection of each fecal sample was examined by floatation technique using saturated saline, with coccidian oocysts per gram (OPG) quantified using modification of McMaster technique (Wang et al., 2010).

Each sample was performed five times, and oocyst number of every sample was expressed using the sum number counted in two chamber of McMaster slide multiplied by the dilution factor (100) to access the OPG. The final result of each sample was obtained using the mean value of five independent examinations. Furthermore, identification of oocysts species was carried out after sporulation of oocysts by incubating faecal samples in 2.5% (w/v) potassium dichromate at room temperature for 2-5 days. Identification was based on the morphological features of the oocyst and sporocysts (size, shape and presence or absence of a micropyle or polar cap or oocyst residuum) under the 100 x objective, with the aid of taxonomic keys (Soulsby, 1968; Pellerdy, 1974; Levine, 1985; Coudert, 1992).

Besides, coproparazitological processing of faecal samples for Cryptosporidium infection was made by Ziehl-Neelsen staining method modified by Henricksen and Pohlenz (1981) and the examination was performed on the optical microscope with immersion objective.

Data analysis

The significant differences was analyzed by chi- square (kh2) using the Statistical Package for Social Science, version 15.0 (SPSS Inc., Chicago, IL), and p<0.05 was considered significant.

RESULTS

Overall prevalence

The present study showed that the overall prevalence of Eimeria spp. and Cryptosporidium spp. among goats were 65.07% and 6.74%, respectively. Additionally, in this study, there was a significant differences observed in the prevalence of Eimeria infection between the 2 different age categories i.e. young animals with the age up-to 12 months were found to be more infected with Eimeria species (75.6%) than the adult ones (56.7%) as depicted in Table I.

Table I.- Prevalence of Eimeria Species among examined goats.

Total no. of animals###Animals###No. (%)

examined

Kids###111###84 (75.6%)

Female###69###53 (81.53%)

Male###42###31 (73.80%)

###2= 9.8, p = 0.002

Adult###141###80 (56.73%)

Female###123###75 (60.97%)

Male###18###5 (27.77%)

###2= 22.93, p < 0.0001

Total###252###164 (65.07%)

Female###192###128 (66.7%)

Male###60###36 (60%)

In respect to sex wise prevalence, the present investigation concluded that female goats had a higher (66.7%) incidence rate of infection than males (60%) for both kids and adult. This marked differences were found to be statistically significant (kh2=22.93, p<0.0001).

Similarly, goat kids were more susceptible to Cryptosporidium infection as compared to adult with an incidence rate of 10.81% and 3.54% respectively as depicted in Table (6). There was a statistical differences among Cryptosporidium infection and age groups (kh2=5.21, P=0.022).

Table II.- Seasonal prevalence of the recovered Eimeria species

Total no. of animals###Animals###No. (%)

examined

Summer###66###47 (71.21%)

Autumn###57###36 (63.26%)

Winter###62###38 (61.29%)

Spring###67###43 (64.28%)

Total###252###164 (65.07%)

###2= 1.6, p =0.659

Table II illustrated that the highest peak of Eimeria spp. infection was observed during summer season with an infection rate of 71.21% followed by spring (64.28%) and autumn (63.26%) seasons respectively, while the lowest per-cent of infection was recorded during winter season (61.29%). Finally, considering the values corresponding to the sampling periods, there was no statistically significant differences between them (kh2= 1.6, P= 0.659).

The different seven Eimeria species were recovered from the faeces of examined goats, based on their morphological characters namely; E. alijevi (50%), E. arloingi (48%), E. caprovina (38%), E. ninakohlyakimovae (20%), E. hirci (18%), E. jolchijevi (12%) and E. aspheronica (10%) (Table III). Furthermore, the same table concluded that, the most frequent Eimeria species among goats were E. alijevi followed by E. arloingi, E caprovina and E. ninakohlyakimovae, while E. aspheronica and E. jolchijevi in a very low percentage.

Table III.- Prevalence of different Eimeria Species among goats.

###Total###Adult goats###Goat kids

Eimeria###(n=50)###More than###<12

species###No. (%)###12months###months

###(n=31)###(n=19)

###No. (%)###No. (%)

E. alijevi###8 (42.12%)###17 (54.83%)###25 (50%)

E. arloingi###9 (47.37%)###15 (48.49%)###24 (48%)

E. caprovina###5 (26.32%)###14 (45.16%)###19 (38%)

E. nina.###6 (31.57%)###4 (12.90%)###10 (20%)

E. hirci###2 (10.52%)###7 (22.58%)###9 (18%)

E. jolchijevi###1 (5.26%)###5 (16.13%)###6 (12%)

E. aspheronica###2 (10.52%)###3 (9.67%)###5 (10%)

Table IV.- Prevalence of single infection of Eimeria species

Species###No. (%)###Remarks

E. alijevi###6 (37.5%)###Recorded in kids and

###adult

E. nina.###1 (6.26%)###Recorded in adult

E. caprovina###2 (12.5%)###Recorded in adult

E. arloingi###3 (18.75%)###Recorded in adult

E. aspheronica###1 (6.26%)###Recorded in goat kids

E. hirci###3 (18.75%)###Recorded in adult

Total###16 (32%)

Mixed infection###34 (68%)###Faecal sample contain

###from 2-4 Eimeria species

In the present study Eimeria species was not detected as pure infection but always found mixed with other species (68%). Mixed infections involving two, three and four species were encountered and only 32% of the examined samples contained a single Eimeria species (Table IV).

The oocyst count per gram of feces (OPG) was conducted, which revealed that the minimum, moderate and maximum values of OPG was 900, 1540 and 3860, respectively, with a mean of 2100. Majority of the samples (20%) had an OPG value ranging from 800 to 1900, and only few samples (10%) had OPG value above 2000 implying a low infection intensity of this parasite (Table V). Furthermore, the number of oocysts excreted was generally lower in adult goats 1200 OPG, whereas higher number of oocyst per gram (OPG) of feces were found in 3400 kids.

Table VII and Figure 1 shows the main morphological characters of the different Eimeria spp. and Cryptosporidium spp. identified.

Table V.- Intensity of Eimeria species infection

Total no. of###Group 1###Group 2###Group 3

examined animals

50###800###1300###2500

###850###1200###3200

###900###1500###4000

###950###1800###4600

###1000###1900###5000

Average###900###1540###3860

Table VI.- Prevalence of Cryptosporidium species among goats

###Adult goats###Goat kids

Eimeria species###Total###More than###<12

###(n=252)###12months###months

###N (%)###(n=141)###(n=111)

###N (%)###N (%)

Cryptosporidium###12###5 (3.54%)###17 (6.74%)

spp.###(10.81%)

###2= 5.21, p =0.022

DISCUSSION

Reports of Eimeria infections date from the beginning of the last century and means for an appropriate species characterization method have been discussed ever since. Several parameters can be used and new methods have been developed (Morris and Gasser, 2006). However, traditional morphological classification is still useful.

Table VII. Morphological characteristics of identified protozoa species.

###Mean oocyst size###Mean

Eimeria species###Shape###Length###Width###sporocyst###Cap###Oocyst wall###Remarks

###(um)###(um)###size (um)

E. alijevi###Spherical###12-22###10-20###10 x 20###-###Smooth, double###Fig. 1a

E. caprovina###Ovoid###25-35###20-30###13 x 9###-###Smooth, double###Fig. 1b

E. hirci###Ellipsoidal###17-25###15-22###9 x 6###+###Double, smooth###Fig. 1c

E. arloingi###Ovoid###19-42###14-32###12 x 7###+###Smooth, double###Fig. 1d

E. nina###Ovoid###18-25###18-20###9 x 11###-###Smooth, double###Fig. 1e

E. jolchijevi###Pyriform###28-35###20-24###11 x 9###+###Thin, smooth###Fig. 1f

E. aspheronica###Ovoid###25-39###18-30###15 x 10###-###Smooth, double###Fig. 1g

Cryptosporidium###Spherical###4###-###-###-###Smooth###Fig. 1h appeared pink

spp.###on blue background

Duszynski and Wilber (1997) emphasized and encouraged precision in the identification of species and established basic characteristics for an appropriate description of the oocysts while Bandoni and Duszynski (1988) already recommended accuracy and caution in these situations. When these recommendations are not accounted for identification problems arise because of similarities between oocysts structures, as seen with Eimeria of goats and sheep (Vieira, 2002). Furthermore, studies focusing on host specificity are also recommended to properly confirm the identification of the isolated pathogen (Lotze et al., 1961; McDougald, 1979). The present study used only goats with no contact with other ruminant animals. The identification was performed by comparison with original descriptions of the parasites and even some variation in the oocysts size (length and width) could be found. This variation was considered a common issue by previous studies (Balicka- Ramisz, 1999; Hassum and Menezes, 2005).

In addition, morphometric variations can be related to many factors such as host and parasite metabolism (Long and Joyner, 1984).

In the present investigation; the achieved results (65.07 %) were nearly similar to that obtained by Cotteleer and Fameree (1978) in Belgium who recorded that the prevalence rate of Eimeria species was 63%. Similarly, Raote et al. (1987) observed 61.9% infection rate of Eimeria species among goats in India. But on the contrary, Norton (1986); O'Callaghan (1989) who's found that the total incidence rate of Eimeria spp. among goats detected in England and South Australia were 98% and 97%, respectively. This variation might be related to some factors as predisposing causes of infection such as moisture, temperature, different localities, and variation in environmental condition.

Concerning the age and sex, the present observation concluded that female kids (81.53%) and male kids (73.80%) had highest incidence rate than adult female (76.2%) and male (23.8%). These results might be due to the under developed resistance in kids to Eimeria infection and low prevalence among adult goats indicated that the well-developed resistance. Furthermore, infected goats can be potential carriers and may act to increase the severity of infection precipitating the disease in the susceptible group of kids.

Regarding to the seasonal variation, the present investigation showed that the highest peak of Eimeria spp. was recorded during summer season (71.21%) followed by spring (64.28%), autumn (63.26%) and the low per-cent was found during the winter season (61.28%). This result in accordance with that mentioned by Harper and Penzhorn (1999) who found a significant increase in the infection rate of Eimeria spp. during the dry season. This might be due to the differences in humidity, temperature from place to place (variation in environmental condition), and the weather in Qena Governorate, upper Egypt was dry and hot in general as it supported by that mentioned by Smith and Sherman (1994) who mentioned that hot and humid weather is particularly conducive to sporocyst development and out breaks of clinical coccidiosis.

In the present study Eimeria spp. was not detected as pure infection but always found mixed with other species (68%) which suggested that the prevailed condition of polyparasitism Khan et al. (2000). Mixed infections were involving two, three or four species whereas, only 32% of the examined samples contained a single Eimeria species and well supported by Alyousif et al. (1992). These results could be attributed to that healthy goat could support the heavy infection with mixed species but stress factors encourage the onset of the disease, or may be due to the nature of the pasture which usually contaminated by various kinds of parasites.

In general, several Eimeria species occur simultaneously in goats (Levine, 1985). In the present investigation, seven species were identified, while in the other studies more than seven different species had been reported (Abo-Shehada and Abo-Farieha, 2003; Gul, 2007; Balicka-Ramisz et al., 2012). Furthermore, many parasitological studies carried out in goats have shown that E. arloingi, E. alijevi, E. hirci, and E. ninakohlyakimovae were the most common species in Poland (Balicka-Ramisz, 1999), South Australia (O'Callaghan,1989), South Africa (Harper and Penzhorn, 1999), Kenya (Kanyari, 1993), and the Czech Republic (Koudela and Bokova, 1998). In this study, E. alijevi, E. arloingi and E. caprovina were the most prevalent species. Coccidia of small ruminants are thus present worldwide and it seems difficult to say that there is any particular geographical distribution for one or the other species of coccidia.

Additionally, it is known that pathogenicity is variable for different Eimeria species. Eimeria arloingi is regarded as one of the most pathogenic species in goats together with E. ninakohlyakimovae (Charter and Paraud, 2012), again indicating the possible high risks for goats around Qena region.

In respect to Cryptosporidium; the present result (6.74 %) was lower as compared to that recorded by Khalil (2000) who found that the total incidence (29.1%) of Cryptosporidium at Delta region, Egypt .This variation might be due to the environmental factors.

Regarding to the age wise prevalence, the present survey recognized that kids were more susceptible to Cryptosporidium infection than adult with total incidence rate 10.81% and 3.54%, respectively. These results were in line with that mentioned by Gorman et al. (1989) who reported that the incidence of Cryptosporidium infection among kids in Chile was 10.5%. Likewise, Kaminjolo et al. (1993); Munoz et al. (1994) found that Cryptosporidium oocysts in goat kids were 13.3% and 20%, respectively. These results might be due to under developed immunity of kids to the parasitic infection.

CONCLUSION

The present study indicated that Eimeria spp. as single or mixed infections are more prevalent parasitic species in the examined region. The implementation of a routine diagnostic strategy can be useful in maintaining Eimeria populations under monitoring and will enable the determination of its potential impact on goat herds in southern Egypt. Furthermore, there had been few studies related to prevalence of cryptosporidiosis in goats, but a thorough and detailed investigation towards the epidemiology of Cryptosporidium spp. in goats are very important to Egypt to assess the potential risk of zoonotic transmission of goat Cryptosporidium spp. to human as the importance of goat as food animal is ever increasing.

ACKNOWLEDGMENTS

We thank the reviewers for their time to carefully review our manuscript. We believe that their positive comments substantially improved this article. Author is also grateful to the Deanship of scientific research, Najran University for supporting and funding this research.

Statement of conflict of interest

Author has declared no conflict of interest.

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Author:El-Shahawy, Ismail Saad
Publication:Pakistan Journal of Zoology
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Date:Oct 31, 2016
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