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Ovine coccidiosis and associated risk factors in Minya, Egypt

Beni-Suef University Journal of Basic and Applied Sciences volume 11, Article number: 137 (2022) Cite this article

Abstract

Background

Coccidiosis is a potential protozoal disease of economic importance in sheep worldwide. The current study aimed to detect the prevalence of ovine coccidiosis and identification of the recovered species in Minya, Egypt. Three hundred and fifty sheep from Minia, Egypt, were coprologically examined for the occurrence of Eimeria species oocysts by using the standard floatation technique.

Results

Oocysts were detected in 180 (51.43%) animals. Mixed infection was recorded in 37.14% (130/350) and single infection was revealed in 14.29% (50/350) sheep. The prevalence of coccidiosis was significantly higher in young sheep. Fourteen Eimeria species were detected; Eimeria bakuensis, E. webybridgensis, E. ahusta, E. intricata, E. granulosa, E. faurei, E. ninakohlyakim-ovae, Eimeria coitae-like, E. parva, E. pallida, E. marsica, E. crandallis, E. ovinoidalis and E. arloingi. The most predominant Eimeria species was Eimeria parva (14.57%; 51/350) followed by E. ovinoidalis (14.0%; 49/350), E. granulosa (8.29%; 29/350), E. bakuensis (7.14%; 25/350), E. intricata (5.43%; 19/350), E. faurei and E. webybridgensis (4.86%; 17/350 each), E. pallida (4.0%; 14/350), E. ninakohlyakim-ovae (3.71%; 13/350), E. crandallis and E. ahsata (3.43%; 12/350 each), E. marsica and E. arloingi (1.71%; 6/350 each). The least abundant species was E. coitae-like (1.14%; 4/350).

Conclusion

Fourteen Eimeria species were recovered from sheep in Minya, Egypt; Eimeria bakuensis, E. webybridgensis, E. ahusta, E. intricata, E. granulosa, E. faurei, E. ninakohlyakim-ovae, Eimeria coitae-like, E. parva, E. pallida, E. marsica, E. crandallis, E. ovinoidalis and E. arloingi. Eimeria parva was the most common while E. coitae-like was the least. To the best of our knowledge, this is the first report for the occurrence of E. coitae-like in sheep in Egypt. Prevention and effective control programs should be strictly followed to avoid economic losses resulted from the coccidian infection.

1 Background

In the underdeveloped countries, small ruminants, particularly sheep, are of a great economic importance as they capable to survive and produce in poor environments, or even reared on low-cost feeds providing an appropriate target for small families in those countries achieving meat and wool as wells as traditional pastoralism [1, 2]. In Egypt, the estimated sheep population is approximately 5.5 million [3]. Coccidiosis of small ruminants is a protozoan infection caused by coccidia parasites of the genus Eimeria which develop in the small and the large intestine of infected animals and affect young animals in particular. Several species of Eimeria are involved in different ruminant hosts, but there is no cross infection due to the strict host specificity. Coccidiosis is of great eco-nomic importance because of the losses due to clinical disease (diarrhoea) and subclinical infections as well (poor weight gain in particular).

Parasites of livestock, including sheep, cause diseases of a major global socio-economic importance [4]. Parasites of the genus Eimeria (Apicomplexa: Eimeriidae) are considered an important cause of the intestinal infection, coccidiosis [5,6,7]. Eimeria parasites usually affect young animals aged up to 4 months, and also they occur in adult animals, acting as reservoirs of the infection [8]. The ingestion of oocysts-infected food and water is the main source of spreading the parasite. Coccidiosis clearly elucidate various clinical signs, such as weight loss, fever, diarrhea (often bloody), dehydration, pale mucous, and even death [9, 10]. The disease might occur in clinical/subclinical form [11]. Clinical coccidiosis often induces potential losses for producers due to costs of medical treatment, adversely affected growth performance and sometimes death of lambs aged less than 3 months [12,13,14]. A high mortality rate is might be common in animals suffering from heavy bloody diarrhea [15]. Overall, coccidiosis is drastically expected when bloody diarrhea, poor body conditions, remarkable weight loss and abdominal pain [16]. Pushing towards the improvement of body conditions and managemental care is mandatory needed to control the disease. The parasite has two phases of biology; endogenous and exogenous phases. During the first, the parasite undergoes multiple divisions in the enterocytes. Sheep ingest sporulated oocysts via contaminated feed/water. Sporulated oocysts release sporozoites in the intestinal lumen. The exogenous phase occurs in the environment [15]. Once coccidiosis has been diagnosed, the treatment of affected sheep mostly not effective, but the severity might be reduced with the early treatment by anticoccidial drugs like toltrazuril, diclazuril and sulfaquinoxaline [15].

The identification of Eimeria species often based on both morphological and molecular features [17]. The molecular approach is disadvantageous as it requires specific tools and high-cost facilities [18]. Therefore, morphological characterization utilizing morphometry of oocysts has been established as a practical and reliable tool for species differentiation [17, 19]. So far, 15 Eimeria species parasitizing sheep have been described [20]. Among those, E. ovinoidalis and E. crandallis are considered as pathogenic species with clear clinical signs of the disease [17]. Other species like E. ahsata, E. marsica, E. bakuensis, E. granulosa and E. parva have been recorded with a little evidence about the pathogenicity of them [12, 21].

The conventional control strategy is achieved by careful husbandry combined with in-feed anticoccidial drugs or vaccination with live or attenuated parasites. It is very urgent to develop safe and effective multivalent vaccine against mixed infection of all the economically important species of Eimeria.

Herein, we aimed to determine the prevalence of different Eimeria spp. in sheep obtained from Minya province, Egypt and morphological identification of the recovered Eimeria species as well as their associated risk factors.

2 Methods

2.1 Study area and animals

Fresh fecal specimens were collected from 350 sheep of various ages and genders allocated sporadically in small flocks kept in households in rural areas (average 4–15 animals/flock) owned by farmers in several districts of Minya province (coordinates: 28°07′10″N 30°44′40″E), Egypt during the period from October 2020 to September 2021. The age of animals was categorized as 0–6 months, 6–12 months and 2–3 years.

2.2 Specimens collection and laboratory examination

Fecal samples were collected directly from the rectum by using sterile disposable gloves. After labeling, containers were transported via cool box dry ice packs to the laboratory of Parasitology, Faculty of Veterinary Medicine, Beni-Suef University, Egypt. These were kept at 4 °C in a refrigerator until used. Fecal samples were parasitologically examined by the use of standard flotation technique to demonstrate oocysts of Eimeria spp. as follows: Approximately 5 g feces from each animal were well mixed with 10 ml of fully saturated salt solution in a plastic cup. The mixture was strained through a tea strainer to discard the fecal debris. Then, the solution was poured into a 15-ml centrifuge tube then the flotation solution was added to the tip of tubes which were closed with cover slips. Tubes underwent centrifugation at 3000 rpm for 2 min and spinning, then, they allowed settling down. The flotation solution was added to the test tube till a reverse meniscus on the surface layer of this solution was formed, then clean dry cover slips were placed on the rim of tubes for 5 min then removed and examined microscopically using various magnifications [3, 22, 23].

2.3 Measurement of oocysts

The calibration of the microscope was done according to Conway and Mckenzie [24]. Briefly, using the low power of the compound microscope, the stage micrometer lines were brought into focus and adjusted the zero line of the stage micrometer to coincide with the zero line of the ocular micrometer. Another line on the ocular micrometer which exactly coincides with a second line on the stage scale was found. The number of spaces between the two lines was counted using the ocular scale and divided this number into the number of microns represented between the two lines on the stage (number of small spaces × 10 microns).

2.4 Statistical analysis

Data were analyzed using a Microsoft Excel worksheet for Windows 2010. Data were summarized by descriptive statistics for the overall prevalence in sheep. The Chi square test was used to analyze the effect of risk factors; age, sex and seasons, on the overall coccidial infections. Variables were significant at P ≤ 0.05 [3, 15, 25].

3 Results

The current study revealed that Eimeria spp. oocysts were recorded in 180 (51.43%) out of 350 fecal samples obtained from sheep of different ages and sexes. Mixed infection was found in 37.14% (130/350) and single infection was revealed in 14.29% (50/350) (Table 1; Fig. 1). The prevalence of coccidiosis significantly varied according to the age; the highest infection rate was in young sheep aged less than one year (92/125; 73.6%) followed by yearlings (35/58; 60.34%) and the lowest one was in adults (53/167; 31.74%) (Table 2). The prevalence was higher in female sheep (113/200; 56.50%) rather than males (67/150; 44.67%). The highest prevalence was revealed in cold season (98/132; 74.24%) rather than that in the hot season (82/218; 37.61%).

Table 1 The overall prevalence of the coccidian infections among the examined sheep
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Fig. 1
figure 1

The overall prevalence of the coccidian infection among the examined sheep

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Table 2 The overall prevalence of coccidian infections relative to the age of sheep
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Fourteen Eimeria spp. were identified; E. ovinoidalis, E. crandallis, E. pallida, E. faurei, E. webybridgensis, E. bakuensis, E. granulosa, E. ahsata, E. parva, E. intricata, E. ninakohlyakim-ovae, E. arloingi, E. coitae-like and E. marsica. Eimeria parva was the most predominant species (51/350; 14.57%) followed by E. ovinoidalis (49/350; 14.0%), E. granulosa (29/350; 8.29%), E. bakuensis (25/350; 7.14%), E. intricata (19/350; 5.43%), E. faurei and E. webybridgensis (17/350; 4.86% each), E. pallida (14/350; 4.0%) E. ninakohlyakim-ovae (13/350; 3.71%), E. crandallis and E. ahsata (12/350; 3.43% each), E. marsica and E. arloingi (6/350; 1.71% each). The least abundant Eimeria species was E. coitae-like (4/350; 1.14%) (Table 3). Morphological features of the revealed Eimeria spp. oocysts were included in Table 4 (Figs. 2, 3, 4).

Table 3 The recovered Eimeria species in feces of the examined sheep
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Table 4 Morphological criteria of recovered ovine Eimeria species
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Fig. 2
figure 2

Morphology of 3 Eimeria species recovered from examined sheep. a Eimeria bakuensis unsporulated oocyst. Note the distinct polar cap (arrow). b Eimeria bakuensis sporulated oocyst. c Eimeria weybridgensis unsporulated oocyst. Note an ellipsoidal to a spherical shape with a smooth wall (arrow). d Eimeria weybridgensis sporulated oocyst. e Eimeria ahsata unsporulated oocyst. Note the smooth wall with yellowish brown coloration (arrow). f Eimeria ahsata sporulated oocyst. (Scale bar = 10 µm)

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Fig. 3
figure 3

Morphology of 5 Eimeria species recovered from examined sheep. a Eimeria intricata unsporulated oocyst. Note a thick and striated oocystic wall (arrow) as well as distinct micropyle and polar cap (arrowhead). Scale bar = 20 µm. b Eimeria granulosa unsporulated oocyst. Note a spherical-shaped sporont with densely granular cytoplasm (arrow). Scale bar = 20 µm. c Eimeria faurei unsporulated oocyst. Note a distinct micropyle without polar cap. Scale bar = 20 µm. d Eimeria ninakohlyakimovae unsporulated oocyst. Note the lack of micropyle and polar cap (arrowhead). Scale bar = 10 µm. e Eimeria cotiae-like unsporulated oocyst. Note striated and brownish coloration of the cyst wall with no micropyle or polar cap (arrowhead). Scale bar = 10 µm. f Eimeria cotiae-like unsporulated oocyst. Note the beginning of sporont division (arrow). Scale bar = 10 µm

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Fig. 4
figure 4

Morphology of 6 Eimeria species recovered from examined sheep. a Eimeria parva unsporulated oocyst. Note the lack of micropyle and polar cap. Inset: The sporulated oocyst has ovoid sporocyst, each sporozoite has central vacuole Scale bar = 25 µm. b Eimeria pallida unsporulated oocyst. Note the imperceptible micropyle (arrowhead). c Eimeria marsica unsporulated oocyst. Note the inconspicuous micropyle (arrowhead). d Eimeria crandallis unsporulated oocyst and sporulated oocyst. Inset: The sporulated oocyst has rounded or ovoid sporocyst and each has two vacuoles Scale bar = 25 µm. e Eimeria ovinoidalis unsporulated oocyst. Note the presence of micropyle without a polar cap (arrowhead). f Eimeria arloingi unsporulated oocyst. Note a distinct micropyle and the polar cap is lid-like and easily dislodged (arrowhead). Scale bar = 10 µm. Inset: The sporulated oocyst has elongated sporocysts and their sporozoite has large vacuole at the broad end. Scale bar = 25 µm

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4 Discussion

Eimeria species are the major cause of coccidiosis in livestock inducing massive economic losses in farm animals largely, reduction in milk and meat, weakness, as well as potential mortality rates [26]. In the present study, out of 350 fecal samples from sheep of various sexes and ages, 180 (51.43%) were infected with Eimeria spp. In Egypt, such result more or less coincided with those revealed by El-Akabawy [27] and Boshra [28] in Kaloubia, Nasr et al. [29] in Sharkia, Bkheet et al. [30] in Beharia, Ramadan et al. [14] in Kaloubia, Mahmoud et al. [31] in Assuit, Mohamaden et al. [7] in Suez and El-Alfy et al. [3] in Dakahlia who recorded infection rates 80.4, 80.76, 76.51, 70, 72.5, 65, 57.7 and 68.4%, respectively. Similarly, in Iraq, Sulaiman et al. [32] detected that the prevalence of coccidiosis was 60.5%. However, in Egypt, the current findings were higher than those previously reported by Mahran [33] in Red Sea, Abouzeid et al. [34] in Sinai and Sultan et al. [35] in Kafr-Elsheikh (6.61, 6.7 and 16.52%, respectively). Furthermore, Toulah [36] in Saudi Arabia, Abakar [37] in Sudan and Majeed et al. [38] in Kuwait recorded infection rates 41, 41.2 and 17.5%, respectively). On the other hand, it was lower than those noted by Bastauerous et al. [39] in Assuit, Egypt and Ali [40] in Sudan who revealed prevalences of 94.9% and 86% among examined sheep. Such difference may be due to changes in environmental condition.

Currently, single infection was recorded in 14.29% (50/350) of infected sheep, while mixed infection rate was found in 37.14% (130/350). Such finding was concomitant with that recorded by El-Akabawy [27] in Kaloubia, who found that mixed infection with more than two Eimeria species was 78.8%, Mohamaden et al. [7] who detected that the mixed infection was 68.3% of the examined sheep in Suez, Ramadan et al. [14] who demonstrated that the mixed infection was 43.7% in Kalubia and El-Alfy et al. [3] who found that the mixed infection was 73.0% in Dakahlia. Moreover, Toulah [36] in Saudi Arabia noticed that the mixed infection with three Eimeria species was 51.22%. On the other hand, the present finding disagreed with that observed by El-Akabawy [27] in Kaloubia, who revealed that the single infection rate was 1.7% among examined sheep. Boshra [28] detected that sheep infected with single Eimeria species was 3.03%, double mixed species was 17.63% while mixed infection with more than two species was 79.33% among examined sheep in different localities in Egypt. Meanwhile, in Sudan, Ali [40] elucidated that mixed infection was in 83%. In Saudi Arabia, Toulah [36] noticed that mixed infection with two Eimeria species was 36.59%.

Concerning the age, the highest infection rate was revealed among sheep aged less than one year (73.6%), followed by those aged one year (60.3%). While the lowest infection rate was found in animals aged 2–3 years (31.7%). This results agreed with that noted by Nasr et al. [29] in Sharkia, Egypt, who detected that the prevalence was higher in young-aged animals (38.09%), followed by immature (24.38%), while the lowest prevalence was found in adult animals (18.30%). Similarly, Muhammed et al. [41] reported that a higher infection rate was observed in young animals (51.56%) than adult ones (15.53%), Ramadan et al. [14] revealed a higher infection rate in young animals (73.6%) than adults (55.6%) and El-Alfy et al. [3] who noted that the highest prevalence was detected in lambs, followed by sheep aged one year and the lowest rate was seen in adults. In the south eastern Ethiopia, Dabasa et al. [42] found that young-aged sheep was more susceptible (21.4%) to the infection than adults (10.8%). On the other hand, the prevalence of the current eimeriosis disagreed with that reported by El-Akabawy [27] in Kaloubia, who found that adult sheep aged 6–12 months were highly susceptible to the infection (89.2%), followed by those aged less than 6 months (79.2%), Abouzeid et al. [34] in Sinai (9.2% in adults and 8.6% in lambs) and Mahmoud et al. [31] in Assuit, Egypt, who observed a high prevalence of Eimeria spp. (65.26% in adults and 63.63% in lambs). Interestingly, Kheirandish et al. [43], Gizachew et al. [44], Rizwan et al. [45] and Yonas and Goa [46] detected that the age of sheep non-significantly affected the infection rate. Such discrepancy might be attributed to the used rearing system of sheep or as result of the development of resistance against Eimeria species in relative to the age.

Regarding to the sex, non-significantly, the infection rate was higher in females (56.5%; 113/200) compared to males (44.67%; 67/150). Such finding went parallel to that recovered by El-Akabawy [27] in Kaloubia who recorded that females were more susceptible to the infection (82.3%) than males (78%), and Mohamaden et al. [7] in Suez, who recorded that females showed a higher prevalence (69.1%) than males (48.4%), Ramadan et al. [14] in Kalubia who found that females were more susceptible to coccidiosis (76.3%) than males (68.3%). They attributed the higher infection rate in females to the hormonal imbalance during both pregnancy and lactation. El-Alfy et al. [3] in Dakahlia who recorded that females showed a higher infection rate (71.8%) than males (59.1%). Conversely, Sulaiman et al. [32] observed that the highest infection rate was 58.3% in males and 37.11% in females, Idris et al. [47] elucidated that male lambs were more susceptible (4.66%) to the infection than females (4.15%) and Dabasa et al. [42] recorded a higher infection rate in males (31%) than females (10.4%). While Ali [40], Yakhchali and Rezaei [48], Gizachew et al. [44], Lakew and Seyoum [49], Yonas and Goa [46] recorded that the sex of sheep had no significant effect on the prevalence of Eimeria spp. In the authors' opinion, the higher prevalence of coccidiosis in female sheep might be referred to the nature of immune status of females as well as the stress caused by pregnancy and lactation.

Furthermore, the present study showed that the prevalence of infection was higher during the cold wet season (74.24%) and lower during the hot dry one (37.61%). Those findings were in agreement with those revealed by Maingi and Munyua [50], Abakar et al. [37] Ramadan et al. [14], Al-Alfy et al. [3] and Ali [40]. The later noted that the highest infection rate occurred in spring (98%), while the lowest rate was in summer (2%). In addition, Nasr et al. [29] in Sharkia, noticed that the highest prevalence was recorded in winter (78.89% and 90.82% for males and females, respectively). Mahran [33] in Red sea, Egypt, found a higher prevalence in winter than that in the summer. On the other hand, El-Akabawy [27] reported that the infection rate was higher in the autumn (89.3%) followed by winter (82.7%), summer (77.4%) and spring (73.9%). Also, Boshra [28] recorded that infection rates were 91.04, 78.57, 74.54 and 74.45% in summer, spring autumn and winter, respectively. Similarly, in Suez, Egypt, Mohamaden et al. [7] detected that the highest infection rate was found in the summer followed by autumn and spring while the lowest rate was seen in winter. However, Maingi and Munyua [50] in Kenya and Kheirandish et al. [43] in Iran reported that there was no significant difference among seasons. The high prevalence of the infection during the cold wet season might be attributed to variations of climatic conditions in such a way that the sporulation and survival of coccidian oocysts are encouraged.

In the present work, fourteen Eimeria species were recovered based on the morphometry of the oocysts using the direct microscopy including E. ovinoidalis, E. crandallis, E. ahsata, E. weybridgensis, E. bakuensis, E. intricata, E. faurei, E. pallida, E. granulosa, E. parva and E. marsica, E. ninakohlyakim-ovae, E. arloingi and E. coitae-like. In Egypt, El-Magdoub et al. [51] recorded 10 ovine Eimeria species; E. ovinoidalis, E. crandallis, E. ahsata, E. bakuensis, E. intricata, E. faurei, E. pallida, E. granulosa, E. parva and E. arloingi. Similarly, Mohamaden et al. [7] revealed the same species. In the same year, Ramadan et al. [14] recovered 8 species; E. ovinoidalis, E. crandallis, E. ahsata, E. intricata, E. faurei, E. pallida, E. granulose and E. parva. Recently, El-Alfy et al. [3] revealed 11 Eimeria species in sheep; E. ovinoidalis, E. crandallis, E. ahsata, E. weybridgensis, E. bakuensis, E. intricata, E. faurei, E. pallida, E. granulosa, E. parva and E. marsica. In countries of similar topographical conditions, In Saudi Arabia, Toulah [36] reported 4 Eimeria species (E. parva, E. intricata, E. arloingi and E. ovina). In Sanandaj, Iran, Yakhchali and Gholami [52] detected 6 Eimeria species (E. ovinoidalis, E. faurei, E. ahsata, E. parva, E. ovina, E. intricata). Moreover, Yakhchali and Zarei [53] recognized 6 Eimeria species (E. intricata, E. ovina, E. faurei, E. parva, E. ahsata and E. pallida) in Tabriz province. In Kuwait, Majeed et al. [38] revealed similar findings. In Germany, Dittmar et al. [54] identified 12 Eimeria species of sheep. To the best of our knowledge, E. coitae-like was first described in sheep in Egypt.

5 Conclusions

Ovine coccidiosis is a potential disease of veterinary importance. The overall prevalence of ovine coccidiosis was 51.43%. The current study revealed 14 Eimeria species; E. ovinoidalis, E. crandallis, E. ahsata, E. weybridgensis, E. bakuensis, E. intricata, E. faurei, E. pallida, E. granulosa, E. parva and E. marsica, E. ninakohlyakim-ovae, E. arloingi and E. coitae-like. Among those, E. coitae-like is recorded for the first time. Mixed infection was found in 37.14% (130/350) and single infection was revealed in 14.29% (50/350). The prevalence of coccidiosis significantly varied according to the age; the highest infection rate was in young sheep aged less than one year (92/125; 73.6%) followed by yearlings (35/58; 60.34%) and the lowest one was in adults (53/167; 31.74%). The prevalence was higher in female sheep (113/200; 56.50%) rather than males (67/150; 44.67%). The highest prevalence was revealed in cold season (98/132; 74.24%) rather than that in the hot season (82/218; 37.61%). The occurrence of the disease is basically related to the ingestion of oocysts in both foodstuffs and the surrounding utensils. The proper management and hygiene during rearing of lambs and adults are mandatory to avoid ovine coccidiosis. Subsequently, more studies are needed to clarify the transmission dynamics depending on the multilocus genetic analysis of different Eimeria species infecting sheep and other ruminant animals.

Availability of data and materials

All data generated or analyzed during this study are included in this published article.

References

  1. FAO (2015) Africa sustainable livestock 2050 report, Country brief Egypt. www.fao.org/3/a-i7312e/pdf. Accessed Sept 2019

  2. Ahmed J, Duguma A, Regassa D, Belina D, Jilo R (2017) Gastrointestinal nematode parasites of small ruminants and anthelmintics efficacy test in sheep of Haramaya District, Eastern Ethiopia. Vet Anim Sci 5(3):39–44. https://doi.org/10.11648/j.avs.20170503.11

    Article  Google Scholar 

  3. El-Alfy E, Abbas I, Al-Kappany Y, Al-Araby M, Abu-Elwafa S, Dubey JP (2020) Prevalence of Eimeria species in sheep (Ovis aries) from Dakahlia governorate, Egypt. J Parasit Dis 44(3):559–573. https://doi.org/10.1007/s12639-020-01229-1

    Article  PubMed  PubMed Central  Google Scholar 

  4. Roeber F, Jex AR, Gasser RB (2013) Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance—an Australian perspective. Parasit Vectors 6:153. https://doi.org/10.1186/1756-3305-6-153

    Article  PubMed  PubMed Central  Google Scholar 

  5. Silva LMR, Muñoz Caro T, Rüdiger G, Vila-Viçosa MJM, Cortes HC, Hermosilla T, Taubert A (2014) The apicomplexan parasite Eimeria arloingi induces caprine neutrophil extracellular traps. Parasitol Res 113(8):2797–2807. https://doi.org/10.1007/s00436-014-3939-0

    Article  PubMed  Google Scholar 

  6. Ahmad TA, Tawfik DM, Sheweita SA, Haroun M, El-Sayed LH (2016) Development of immunization trials against Acinetobacter baumannii. Trials Vaccinol 5:53–60. https://doi.org/10.1016/j.trivac.2016.03.001

    Article  Google Scholar 

  7. Mohamaden WI, Sallam NH, Abouelhassan EM (2018) Prevalence of Eimeria species among sheep and goats in Suez Governorate. Egypt Int J Vet Sci Med 6(1):65–72

    Article  PubMed  Google Scholar 

  8. Lopes WDZ, Borges FDA, Faiolla TDP, Antunes ITA, Borges DGI, Rodriguez FDS, Feraro GFR, Texcira WFO (2013) Eimeria species in young and adult sheep raised under intensive and/semi intensive system of a herd from Umuarama city, Parana state, Brazil. Agencia Rur Santa Maria 43(11):2031–2036. https://doi.org/10.1590/S0103-84782013001100018

    Article  Google Scholar 

  9. Andrade ALF Jr, Silva PC, Aguiar EM, Santos FG (2012) Use of coccidiostat in mineral salt and study on ovine eimeriosis. Rev Bras Parasitol Vet 21(1):16–21. https://doi.org/10.1590/S1984-29612012000100004

    Article  PubMed  Google Scholar 

  10. Keeton ST, Navarre CB (2018) Coccidiosis in large and small ruminants. Vet Clin N Am Food Anim Pract 34(1):201–208. https://doi.org/10.1016/j.cvfa.2017.10.009

    Article  Google Scholar 

  11. Lagares AFBF (2008) Parasites de pequenos ruminant esnaregiao da cova da Bara (Dissertacao). Faculdade de Medicma Veterinaria Universidade Tecnica de Lisboa, Lisboa

    Google Scholar 

  12. Reeg KJ, Gauly M, Bauer C, Mertens C, Erhardt G, Zahner H (2005) Coccidial infection in housed lambs: oocysts excretion, antibody levels and genetic influence on the infection. Vet Parasitol 127:209–219. https://doi.org/10.1016/j.vetpar.2004.10.018

    Article  PubMed  Google Scholar 

  13. Elmadawy RS, Elkhaiat HM (2014) Efficacy of clindamycin, yeast (Saccharomyces cerevisiae) and clindamycin-Saccharomyces cerevisiae combination versus toltrazuril on experimentally induced coccidiosis in lambs. Int J Appl Nat Sci 3(5):99–110

    Google Scholar 

  14. Ramadan MY, Elmadway RS, Lashin AI, ELdiarby AS (2018) Prevalence of Eimeria species in sheep with a special reference to vaccinated pregnant ewes for maternal immunity for the first time. Benha Vet M J 34(3):218–231. https://doi.org/10.21608/BVMJ.2018.44747

  15. Kareem SI, Yücel ŞY (2015) Prevalence of Eimeria species in sheep in Sulaimaniya province, Iraq. J Entomol Zool Stud 3(4):317–322

    Google Scholar 

  16. Pattison M, McMullin P, Bradbury J, Alexander D (2007) Poultry disease, 6th edn. Butterworth, India, pp 444–456

    Google Scholar 

  17. de Souza LEB, da Cruz JF, Neto MRT, Albuquerque GR, Melo ADB, Tapia DMT (2015) Epidemiology of Eimeria infections in sheep raised extensively in a semiarid region of Brazil. Rev Bras Parasitol Vet 24(4):410–415. https://doi.org/10.1590/S1984-29612015070

    Article  PubMed  Google Scholar 

  18. Barkway CP, Pocock RL, Vrba V, Blake DP (2011) Loop-mediated isothermal amplification (LAMP) assays for the species-specific detection of Eimeria that infect chickens. BMC Vet Res 7(67):1–8. https://doi.org/10.1186/1746-6148-7-67

    Article  Google Scholar 

  19. Ahid SMM, Medeiros VMC, Bezerra ACDS, Maia MB, Xavier VM, Vieira LS (2009) Scientific note: Species of the genus Eimeria Schneider, 1875 (Apicomplexa: Eimeriidae) in small ruminants in the west mesorregion of the state of Rio Grande do Norte, Brazil. Ciênc Anim Bras 10(3):984–989. https://doi.org/10.5216/cab.v10i3.825

    Article  Google Scholar 

  20. Saratsis A, Joachim A, Alexandros S, Sotiraki S (2011) Lamb coccidiosis dynamics in different dairy production systems. Vet Parasitol 181(2–4):131–138. https://doi.org/10.1016/j.vetpar.2011.04.027

    Article  PubMed  Google Scholar 

  21. Skirnisson K (2007) Eimeria spp. (Coccidia, Protozoa) infections in a flock of sheep in Iceland: Species composition and seasonal abundance. Iceland Agric Sci 20:73–80

    Google Scholar 

  22. Christensen JF (1938) Species differentiation in the coccidia from the domestic sheep. J Parasitol 24(5):453–467

    Article  Google Scholar 

  23. Zajac AM, Conboy GA (2006) Veterinary clinical parasitoloy. Blackwell, New York, pp 3–4

    Google Scholar 

  24. Conway DP, Mckenzie ME (2007) Poultry Coccidiosis: diagnostic and testing procedures. 3rd ed. Blackwell Publishing, Ames, p 164

  25. Hasan KA, Mahmood OI (2021) Prevalence of Eimeria species in sheep and goat in Tikrit City, Iraq. Indian J Forensic Med Toxicol 15(2):2032–2036

    Google Scholar 

  26. Kenyon F, Jackson F (2012) Targeted flock/herd and individual ruminant treatment approaches. Vet Parasitol 186(1–2):10–17. https://doi.org/10.1016/j.vetpar.2011.11.041

    Article  CAS  PubMed  Google Scholar 

  27. El-Akabawy LMI (1993) Studies on coccidia species infecting sheep in Kalubia Governorate. PhD Faculty Vet Med Benha Branch Zagazig Univ

  28. Boshra MA (1994) Some Studies on Coccodiosis in Sheep. Sc. Faculty Vet. Med. Benha Branch, Zag. Univ, M.V

    Google Scholar 

  29. Nasr SSM, Fayek SA, Azazy OME, Amer OH (2008) Studies on protozoa of small ruminants in Sharkia province. PhD Vet Med Sci Zag Univ

  30. Bkheet AA, Fadly RS, Elhoffy HR (2010) Studies on some bacterial and parasitic causes of lamb diarrhea in Behaira province and the subsequent biochemical changes. Assuit Vet Med J 56(127):203–222. https://doi.org/10.21608/AVMJ.2010.174246

    Article  Google Scholar 

  31. Mahmoud HYA, Ali AO, Ali RH, Ahmed AE (2018) Evaluation of clinical status and treatment trails in sheep and goats infested with Eimeria species. Assuit Vet Med J 64(156):123–128. https://doi.org/10.21608/AVMJ.2018.168713

    Article  Google Scholar 

  32. Sulaiman EG, Talib Q, Daham E, Arsalan SH (2005) Study of some eggs and oocysts of internal parasites in sheep Mosul, Iraq. J Vet Sci 19(1):21–32. https://doi.org/10.33899/ijvs.2005.37275

    Article  Google Scholar 

  33. Mahran OM (2009) Prevalence and significance of gastrointestinal parasites in desert sheep in the triangular area (Shalatin-AbuRamaid-Halaeeb) Red sea Governorate, Egypt and trails of treatment. Assuit Vet Med J 55(120):1–23. https://doi.org/10.21608/AVMJ.2009.174199

    Article  Google Scholar 

  34. Abouzeid NZ, Selim AM, El-Hady KM (2010) Prevalence of gastrointestinal parasites infections in sheep in the Zoo garden and Sinai district and study the efficacy of anthelmintic drug in the treatment of these parasites. J Am Sci 6(11):544–551

    Google Scholar 

  35. Sultan K, Elmonir W, Hegaz Y (2016) Gastrointestinal parasites of sheep in Kafrelsheikh governorate, Egypt. Prevalence, control and public health implications. Beni-Suef Univ J Basic Appl Sci 5(1):79–84. https://doi.org/10.1016/j.bjbas.2015.12.001

    Article  Google Scholar 

  36. Toulah HF (2007) Prevalence and comparative morphological study of four Eimeria species of sheep in Jeddah Area. Saudi J Biol Sci 7(2):413–416. https://doi.org/10.3923/jbs.2007.413.416

    Article  Google Scholar 

  37. Abakar MY (2010) Survey of internal parasites in sheep and goat in the White State—Sudan (April–May 2009). Fac Vet Med Khartoum Univ MDV

  38. Majeed QA, Alazemi MS, Hemedi AA, Tahrani LM (2015) Study on parasites from farm animals in Kuwait. J Egypt Soc Parasitol 45(1):71–74. https://doi.org/10.12816/0010851

    Article  PubMed  Google Scholar 

  39. Bastauerous AF, El-Thabet A, Abdel Haeez MM, Sayed AM, Arafa MI (2001) Studies on diarrhea in lambs in Assuit Governorate 1—isolation and identification of causative bacterial and parasitic agents. Assuit Vet Med J 46(91):98–108. https://doi.org/10.21608/AVMJ.2001.180285

    Article  Google Scholar 

  40. Ali AAS (2005) Survey on Eimeria spp. infecting sheep in the Red Sea State, Eastern Sudan. Fac Vet Med Khartoum Univ MDV

  41. Muhammed MM, Yusuf ND, Hassan DI (2017) A survey of endo-parasites of indigenous sheep breeds in Lafia, Nasarawa State. Nigeria J Biol Genet Res 3(1):2545–5710

    Google Scholar 

  42. Dabasa G, Shanko T, Zewdei W, Jilo K, Gurmesa G, Abdela N (2017) Prevalence of small ruminant gastrointestinal parasites infections and associated risk factors in selected districts of Bale Zone, South eastern Ethiopia. J Parasitol Vector Biol 9(6):81–88. https://doi.org/10.5897/JPVB2017.0286

    Article  Google Scholar 

  43. Kheirandish R, Nouroallahi-fard SR, Eslah E (2012) The prevalence and pathology of ovine coccidiosis in Kermen, Iran. Eurasian J Vet Sci 28(4):194–198. https://doi.org/10.1007/s12639-014-0613-5

    Article  Google Scholar 

  44. Gizachew A, Fikadu N, birhanu T, (2014) Prevalence and associated risk factors of major sheep gastrointestinal parasites in and around Bako Town Western Ethiopia. Livest Res Rural Dev 26(10):1–10

    Google Scholar 

  45. Rizwan HM, Sajid MS, Iqbal Z, Squib M (2017) Point prevalence of gastrointestinal parasites of domestic sheep (Ovis aries) in district Sialko Punjab, Pakistan. J Anim Plant Sci 27(3):803–808

    Google Scholar 

  46. Yonas Y, Goa A (2017) Prevalence and associated risk factors of major sheep gastro intestinal parasites in and around Wolaita Sodo, Southern Ethiopia. Int J Curr Res Med 3(3):30–38. https://doi.org/10.22192/ijcrms.2017.03.03.005

    Article  Google Scholar 

  47. Idris A, Moors E, Sohnrey B, Gauly M (2012) Gastrointestinal nematode infection in German sheep. Parasitol Res 110(4):1453–1459. https://doi.org/10.1007/s00436-011-2648-1

    Article  PubMed  Google Scholar 

  48. Yakhchali M, Rezaei AA (2010) The prevalence and intensity of Eimeria spp. infection in sheep of Malayer suburb, Iran. Arch Razi Inst 65(1):27–32.

  49. Lakew A, Seyoum Z (2016) Ovine coccidiosis: prevalence and associated risk factors in and around Addis-Zemen, Northwest Ethiopia. Turk J Vet Anim Sci 40(5):645–650. https://doi.org/10.3906/vet-1509-18

    Article  Google Scholar 

  50. Maingi N, Munyua A (1994) The prevalence and intensity of capital infection with Eimeria species in sheep in Nyandarua district, Kenya. Vet Res Commun 18(1):19–25. https://doi.org/10.1007/BF01839257

    Article  CAS  PubMed  Google Scholar 

  51. El-Magdoub AA, El-Sayed IA, Mahdy AE (1999) Relationship between system of raising Egyptian buffaloes and the effect of climate conditions on the helminthic infection rate, middle Delta, Egypt. J Egypt Soc Parasitol 29(2):505–515

    CAS  PubMed  Google Scholar 

  52. Yakhchali M, Golami E (2008) Eimeria infection (Coccidia: Eimeriidae) in sheep of different age groups in Sanandaj city. Iran Vet Arhiv 78(1):57–64

    Google Scholar 

  53. Yakhchali M, Zarei MR (2008) Prevalence of Eimeria infection in sheep of Tabriz suburb, Iran. Iran J Vet 9(3):277–280

    Google Scholar 

  54. Dittmar K, Mundt HC, Grzonka E, Daugschies A, Bangoura B (2010) Ovine coccidiosis in housed lambs in Saxony-Anhalt (Central Germany). Berl Munch Tierarztl Wochenschr 123(1–2):49–57. https://doi.org/10.2376/0005-9366-123-49

    Article  PubMed  Google Scholar 

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Acknowledgements

Authors all veterinarians and farmers who facilitated collecting fecal specimens.

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Authors and Affiliations

  1. Department of Parasitology, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef, 62511, Egypt

    Hend Ibrahim Mohamed, Waleed M. Arafa & Khaled Mohamed El-Dakhly

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  1. Hend Ibrahim Mohamed
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  2. Waleed M. Arafa
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  3. Khaled Mohamed El-Dakhly
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by all authors. The first draft of the manuscript was written by KME and HIM and all authors commented on previous versions of the manuscript. WMA applied the statistical analysis. All authors read and approved the final manuscript.

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Correspondence to Hend Ibrahim Mohamed.

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Mohamed, H.I., Arafa, W.M. & El-Dakhly, K.M. Ovine coccidiosis and associated risk factors in Minya, Egypt. Beni-Suef Univ J Basic Appl Sci 11, 137 (2022). https://doi.org/10.1186/s43088-022-00318-9

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