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Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2020 May 19;44(3):559–573. doi: 10.1007/s12639-020-01229-1

Prevalence of Eimeria species in sheep (Ovis aries) from Dakahlia governorate, Egypt

El-Sayed El-Alfy 1, Ibrahim Abbas 1,✉, Yara Al-Kappany 1, Moustafa Al-Araby 1, Salah Abu-Elwafa 1, Jitender P Dubey 2
PMCID: PMC7410986  PMID: 32801508

Abstract

Feces from 184 sheep from Dakahlia governorate, Egypt were tested for Eimeria species oocysts by using the standard floatation technique; oocysts were detected in 126 (68.4%). The prevalence was significantly higher in young sheep than adults. Eleven Eimeria species were identified: Eimeria ahsata, Eimeria bakuensis, Eimeria crandallis, Eimeria faurei, Eimeria granulosa, Eimeria intricata, Eimeria marsica, Eimeria ovinoidalis, Eimeria pallida, Eimeria parva and Eimeria webybridgensis. Oocysts of the most pathogenic ovine species, E. ovinoidalis, were detected in 27 (14.6%) sheep. This is the first report of E. webybridgensis in sheep from Egypt, possibly due to close similarity of their oocysts to those of E. crandallis which stated in the earlier reports. Worldwide reports on epidemiology of Eimeria spp. infections in sheep are tabulated.

Keywords: Eimeria, Eimeria ovinoidalis, Coccidiosis, Prevalence, Sheep, Egypt

Introduction

Ovine coccidiosis can be a serious disease with economic consequences (Chartiera and Paraud 2012). Sheep are infected with 1 or more Eimeria spp; of them, E. ovinoidalis and E. crandallis are the most pathogenic species (Gregory et al. 1989). Until 3 decades ago, Eimeria spp. in sheep and goats were considered common. Cross transmission trials revealed that Eimeria in sheep and goats are species specific (McDougald 1979).

In Egypt, the estimated sheep population is 5.5 million (FAO 2015); 25% of them are reared in the Nile Delta region (Thomson et al. 2000). However, no reports on sheep coccidiosis from Dakahlia governorate, the largest agricultural governorate in the Delta region, are available. Additionally, Chartiera and Paraud (2012) reviewed different epidemiological, clinical and control aspects of small ruminants’ coccidiosis; however, no data on the prevalence or the revealed Eimeria species worldwide were included.

Here, we aimed to determine the prevalence of different Eimeria spp. in sheep from Dakahlia governorate, Egypt, and to review reports concerned with the prevalence of this common parasite in sheep worldwide.

Materials and methods

Fresh feces collected from 184 sheep of various ages and genders during August 2015 to July 2016, were tested for oocysts of Eimeria spp. using the standard flotation technique (Duszynski and Wilber 1997). Sheep in this region are raised in small flocks (4–15 animals/flock) kept in households in rural areas of Dakahlia governorate (31° 50′ N, 31° 00′ E), Egypt. Flocks are reared in a nomadic pastoralism system where animals move within the agricultural lands and graze on residues of the harvested crops. Mixing of flocks from different households during grazing is common. Flocks are not treated with any anticoccidial. Sheep were divided into 3 age groups; young (< 1 year old), yearlings (1–2 years) and adults (> 2 years). Eimeria oocysts from positive samples were sporulated at room temperature using 2.5% potassium dichromate. Morphological observations and micrographs of sporulated and non-sporulated oocysts were performed using a binocular microscope coupled to Amscope® camera (Carl Zeiss, Oberkochen, Germany); oocysts’ sizes were measured using a calibrated ocular micrometer. Different Eimeria spp. were identified per Eckert et al. (1995). Results were statistically analyzed using a chi-square test. The 95% confidence intervals of a proportion including continuity correction and odds ratios were calculated using www.vassarstats.net.

Results

Eimeria spp. oocysts were detected in 126 (68.4%) of 184 feces. The prevalence varied with age; the highest prevalence was in young sheep (59/63; 93.6%) followed by yearlings (37/53; 69.8%; OR = 6.38; P = 0.00071) and at least in adults (30/68; 44.1%; OR = 18.68; P ≤ 0.0001). Prevalence was higher in females (97/135; 71.8%) than males (29/49; 59.1%; OR = 1.76; P = 0.102). The highest prevalence was in Autumn (26/33; 78.7%) followed by Spring (22/39; 56.4%; OR = 2.87; P = 045), Summer (23/34; 67.6%; OR = 1.78; P = 0.303), and Winter (55/78; 70.5%; OR = 1.55; P = 0.37).

Eleven Eimeria spp. were identified; of them, E. crandallis/E. webybridgensis (40.2%) and E. bakuensis (33.7%) were the most prevalent. Eimeria ovinoidalis were detected in 14.6% (27/184). The other identified species were E. granulosa, E. ahsata, E. parva, E. intricata, E. pallida, E. faurei and E. marsica. Mixed infections (73.0%: dual 31.7%, triple 30.1%, quadruple 10.3% and quintuple 0.8%) were common than single infections (26.9%), Table 1.

Table 1.

Prevalence of different Eimeria spp. in feces of 184 examined sheep from Dakahlia governorate, Egypt

Eimeria species No. positive (%) Single infection Mixed infection
No. positive (%) No. positive (%)
E. ahsata 26 (14.1) 1 (0.8) 25 (19.8)
E. bakuensis 62 (33.7) 9 (7.1) 53 (42.1)
E. crandallis/E. webybridgensis 74 (40.2) 19 (15.1) 55 (43.6)
E. faurei 12 (6.5) 0.0 12 (9.5)
E. granulosa 27 (14.6) 3 (2.4) 24 (19.1)
E. ovinoidalis 27 (14.6) 1 (0.8) 26 (20.6)
E. intricata 17 (9.2) 0.0 17 (13.5)
E. marsica 5 (2.7) 0.0 5 (3.9)
E. pallida 14 (7.6) 1 (0.8) 13 (10.3)
E. parva 21 (11.4) 0.0 21 (16.6)
Total 126 (68.4) 34 (26.9) 92 (73.0)
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Morphological characteristics of different Eimeria spp. oocysts revealed in the present study (Fig. 1) were like the description of these species in literature (Norton et al. 1974; Eckert et al. 1995).

Fig. 1.

Fig. 1

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Oocysts of Eimeria spp. in feces of sheep from Dakahlia governorate, Egypt. From a to i: Sporulated oocysts of E. ahsata (a), E. bakuensis (b), E. faurei (c), E. granulosa (d), E. intricata (e), E. marsica (f), E. ovinoidalis (g), E. pallida (h), E. parva (i). Non-sporulated oocyst of E. crandallis/E. webybridgensis (j). Sporulated oocyst of E. crandallis (k). Sporulated oocyst of E. webybridgensis (l). Unstained. Scale bars = 10 µm

Discussion

The present study is the first report of different Eimeria spp. in sheep from Dakahlia governorate, Egypt; 126 (68.4%) of 184 were infected. Earlier reports from other Egyptian governorates together with the worldwide reports are summarized in Table 2.

Table 2.

Prevalence of Eimeria species in sheep worldwide

Country/region Age range No. examined No. positive (%) No. of Eimeria spp. Eimeria species and remarks References
Australia
 South regions 3–13 months 136 109 (80.0) 11 E. ahs 31%, E. bak 55%, E. cran/E, weyb 76%, E. fau 24%, E. intr 37%, E. gran 49%, E. ovin 54%, E. par/E, pal 44%, E. pun 1% O’Callaghan et al. (1987)
 Different Variable 3412 616 (18.1) 5

118 positive samples were genotyped (PCR/Sequencing)

E. ahs 28%, E. cran 48.3%, E. ovin 10.1%, E. weyb 10.1%, E. cylindrica 4.2%

No mixed infection

 Yang et al. (2014)
Austria
 Styria Ewes, lambs 60, 126 NS 8

E. ahs 19.1%, E. bak 18.4%, E. cran/E. weyb 27.3%, E. fau 4.8%, E. gran 1.0%, E. ovin 28.3%, E. pal 10.9%, E. par 14.0% in adults

Lambs were infected with same species except E. gran

 Platzer et al. (2005)
Bangladesh
 Different region NS 136 42 (30.8) NS NS Islam and Taimur (2008)
Brazil
 Sao Paolo 2–32 weeks 25 NS 8 E. ahs, E. bak, E. cran, E. intr, E. ovin, E. pal, E. par, E. weyb Amarante and Barbosa (1992)
 Sobral, Ceara Lambs, dams 30,10 NS 9 E. ahs, E. bak, E. caprovina, E. cran, E. fau, E. gran, E. intr, E. ovin, E. par Vieira et al. (1999)
 Mostardas NS 100 59 (59.0) 9 E. ahs 23.72%, E. bak 6.77%, E. cran 5.08%, E. fau 1.69%, E. gran 20.33%, E. ovin 11.86%, E. pal 1.69%, E. par 37.28%, E. pun 23.72% da Silva et al. (2008)
 Rio Grande do Norte 1–90 days 27 17–100% 8 E. ahs 43.3%, E. bak 43.3%, E. cran 65.7%, E. fau 29.0%, E. gran 53.7%, E. intr 3%, E. ovin 48.8%, E. par 54.7% Silva et al. (2011)
 Santa Ines NS 100 63 (63.0) 6 E. arloingi 6%, E. Fau 38%, E. intr 4%, E. ninakohlyakimovae 32%, E. pal 2%, E. par 12%, Martins et al. (2011)
 Lajes 4–8 months 64 36 (56.2) NS NS Souza et al. (2012)
 Colinas Lambs, adults 255 50 (19,6) 8 E. ahs, E. bak, E. cran, E. fau, E. Intr, E. ovin, E. pal, E. par Almeida (2013)
 Parana 1–8 months 210 147 (70.0) 9 E. ahs 8.1%, E. baka 0.6%, E. cran 50%, E. fau 8.1%, E. gran 2.7%, E. intr 5.4%, E. ovinaa 1.3%, E. ovin 2%, E. par 21.6% Lopes et al. (2013)
 Garanhuns 12 months 408 270 (66.1) 8 E. ahs 51.8%, E. bak 54.8%, E. cran 58.9%, E. fau 22.9%, E. gran 56.3%, E. ovin 72.6%, E. pal 14.4%, E. par 64.8%, de Macedo et al. (2019)
Canada
 Alberta NS 211 211 (100.0) 10 E. ahs 86%, E. arloingi 82%, E. cran 88%, E. fau 52%, E. gran 7%, E. intr 14%, E. ninakohlyakimovae 69%, E. pal 6%, E. par 53%, E. pun 4% Mahrt (1969)
 Western region NS 510 461 (90.0) 8 E. ahs 33%, E. bak 56%, E. cran 34%, E. fau 6%, E. gran 1%, E intr 5%, E. ninakohlyakimovae 19%, E. par 35% Uhazy et al. (1971)
Croatia
 North Dalmatia Lambs 49 37 (75.5) 9 E. bak, E. cran, E. fau, E. gran, E. intr, E. mar, E. ovin, E. pal, E. par Šarić et al. (2015)
China Wang et al. (2010)
 Heilongjiang Adults, lambs 309 287 (92.9) 8 E. ahs 67.2%, E. bak 44.3%, E. cran 11.2%, E. fau 17.1%, E. gran 12.9%, E. intr 12.5%, E. pal 3.8%,E. par 59.9%
Columbia
 Tennessee 15 months 23 9 (39.0) 5 E. ahs, E. bak, E. fau, E. gilruthi, E. ovin Ammar et al. (2019)
 Encino, Duitama, and Belen  < 12 to > 24 months 97 30 (30.9) NS NS León et al. (2019)
Czech Republic
 Sokolov Ewes 348 188 (54.0) 4 E. cran/weyb, E. intr, E. ovin, E. par Kyriánová et al. (2017)
Lambs 333 252 (75.7) E. ovin was the most prevalent (84% in ewes and 85% in lambs)
Egypt
 Kalubia 6–9 months 18 13 (72.2) 2 E. cran, E. ovin. 13 lambs had bloody diarrhea Ghanem and Abd El-Raof (2005)
 Sinai Different 240 16 (6.7) NS NS Abouzeid et al. (2010)
 Matrouh 1–60 days 185 98 (52.9) 9 E. ahs 14.6%, E. bak 21.1%, E. cran 49.2%, E. fau 14.1%, E. gran 11.3%, E. intr 8.4%, E. mar 4.8%, E. ovin 36.7%, E. par 30.2% Abou-El-Naga (2010)
 Kafrelsheikh NS 224 37 (16.5) NS NS Sultan et al. (2016)
 Suez  > 6 months 142 82 (57.7) 10 E. ahs 30.5%, E. arloingi, E. bak 26.8%, E. cran 30.5%, E. fau 18.3%, E. gran 14.6%, E. intr 7.3%, E. ovin 12.2%, E. pal 13.4%, E. par 18.3% Mohamaden et al. (2018)
 Dakahlia Different 184 126 (68.4) 11 E. ahs 14.1%, E. bak 33.7%, E. cran/E. weyb 40.2%, E. fau 6.5%, E. gran 14.6%, E. intr 9.2%, E. mar 2.7%, E. ovin 14.6%, E. pal 7.6%, E. par 11.4% Present study
Estonia
 Vormsi, Hiiumaa, and Saaremaa NS 92 herds 87 (94.6) 11 E. ahs 23%, E. bak 50.6%, E. cran 14.9%, E. faur 28.7%, E. gran 26.4%, E. intr 4.6%, E. pal 31.0%, E. par 37.9%, E. mar 2.3%, E. ovin 93.1%, E. weyb 33.3% Lassen et al. (2013)
Ethiopia
 Elfora export abattoir < 1 to 2 years 262 175 (66.8) 12 The most prevalent species were E. cran 30%, E. pal 13.8%, E. par 30.8%, Ayana et al. (2009)
 Bishoftu (Oromia) < 1 to > 1 years 157 78 (49.7) NS NS Bersissa et al. (2011)
 Gechi District < 2 to > 2 years 255 31 (12.2) NS NS Emiru et al. (2013)
 Gemechis and Boke Districts Different 384 121 (31.5) NS NS Daniel et al. (2014)
Germany
 Northwest regions Different 69 100% in < 10 wk 10 E. ahs, E. bak, E. cran /weyb, E. fau, E. gran, E. intr, E. ovin, E. pal, E. par Barutzki et al. (1990)
 All regions NS 374 155 (41.4) NS NS Raue et al. (2017)
Ghana
 Ayeduase Different 110 57 (51.8) NS Lambs had higher prevalence (87.5%) Owusu et al. (2016)
 Coastal Savannah Different 502 387 (77.1) NS Result from sheep and goats are combined together Squire et al. (2019)
Iceland
 Fjárborgir Lambs NS NS 10 E. ahs, E. bak, E. cran, E. fau, E. gran, E. intr, E. ovin, E. pal, E. par, E. weyb Reginsson and Richter (1997)
 Fossárdalur Ewes and lambs NS NS 10 E. ahs 5.6%, E. bak 18.9%, E. cran 1.4%, E. fau 4.2%, E. gran 8.2%, E. intr 1.6%, E. ovin 40.7%, E. pal 1.6%, E. par 6.7%, E. weyb 11.1% Skirnisson (2007)
Iran
 Tabriz < 6 months to > 1 years 240 40 (16.7) 6 E. ahs 8%, E. bak 18%, E. fau 18%, E. par 13%, E. pal 8%, E. intr 35% Yakhchali and Zarei (2008)
 Sanandaj Different 240 46 (19.2) 6 E. ahs 10%, E. bak 10%, E. fau 29%, E. intr 10%, E. ovin 31%, E. par 10% Yakhchali and Golami (2008)
 Malayer Different 250 40 (16.67) 7 E. ahs 6%, E. bak 16%, E. fau 16%, E. intr 39%, E. ovin 4%, E. pal 7%, E. par 12% Yakhchali and Rezaei (2010)
 Kabodan NS 41 33 (80.4) 4 E. ahs 6.5%, E. fau 6.5%, E. ovin 9.7%, E. par 32.3%. wild sheep Tavassoli and Khoshvaghti (2010)
 Kermanshah and Ilam Adult, lambs 410 375 (91.5) 10 E. ahs 81.8%, E. bak 56.2%, E. cran 33.06%, E. fau 24.8%, E. gran 2.93%, E. intr 15.2%, E. ovin 41.6%, E. pal 58.4%, E. par 67.4%, E. weyb 5.06%, Hashemnia et al. (2014)
 Rudsar Different 270 170 (63.0) 5 E. ahs, E. bak, E. cran, E. ovin, E. par Nourollahi-Fard et al. (2016)
 Zabol Different 420 84 (20.0) 6 E. ahs 8.3%, E. intr 0.9%, E.ovin 3.5%, E. pal 2.8%, E. par 7.3%, E. weyb 2.1%, Mirzaei et al. (2016)
India
 Karnataka NS 300 120 (40.0) NS NS Mamatha and D'Souza (2007)
 Mathura Different 596 208 (34.9) 5 E. bak 27.6%, E. fau 11.24%, E. intr 0.11%, E. ovin 11.1%, E. par 15.4%, Om et al. (2010)
 Rajasthan NS 3964 2010 (50.7) NS NS Swarnkar et al. (2010)
 Maharashtra NS 2462 594 (24.1) 10 E. ajantai 5.7%, E. ahs 9.2%, E. bak 6.9%, E. balloonii 4.3%, E. beedatus 3.7%, E. cran 18.2%, E. intr 10.2%, E. ninakohlyakimovae 12.6%, E. par 15.1%, E. weyb 13.8% More et al. (2011)
 Kashmir 12–89 months 500 49 (9.8) NS NS Bhat et al. (2012)
 Andhra Pradesh NS 150 7 (4.6) 2 E. granulose, E. parva Murthy and Rao (2014)
 Omerga NS 127 92 (72.4) NS NS Sontakke et al. (2015)
 Karnataka 6–9 months 47 42 (89.3) 8 E. ahs, E. arloingi, E. bak, E. fau, E. gran, E. intr, E. ovin, E. par. Outbreak with bloody diarrhea and mortalities in lambs Adeppa et al. (2016)
 Jalpaiguri < 1 to > 3 years 1350 431 (31.9) NS NS Molla and Bandyopadhyay (2016)
Iraq
 Baghdad NS 306 230 (75.1) 9 E. bak, E.cran, E.fau, E. gran, E. mar, E. ovin, E. pal, E. par, E. weyb Fadl et al. (2011)
 Mosul Different 500 318 (63.6) 9 E. ahs 65.4%, E. bak 86.7%, E. cran 30.5%, E. fau 19.8%, E. gran10%, E. intr 11%, E. ovin 73.5%, E. pal 38.9%, E. par 56.6% Hasan and Abed (2012)
 Baghdad NS 280 195 (69.6) NS E. bak (18.4%) was the highest and the lowest was E. arloingi (1.5%) Kalef et al. (2013)
 Diyala Different 143 124 (86.7) 8 E. ahs 22.6%, E. cran 18.8%, E. fau 3.77%, E. gran 16.1%, E. intr 8.5%, E. ovin 6.6%, E. pal 10.3%, E. par 13.2% Minnat (2014)
 Sulaimaniya Different 150 108 (72.0) 11 E. ahs 23.1%, E. bak 33.3%, E. cran 25%, E. fau 23.1%, E. gran 14.81%, E. intr 32.4%, E. mar 25.9%, E. ovin 35.2%, E. pal 50.9%, E. par 53.7%, E. weyb 26.8%, Kareem and Yücel (2015)
 Wasite NS 120 69 (57.5) 10 E. ahs 22.5%, E. bak 20%, E. cran 11.6%, E. fau 12.5%, E. gran 3.3%, E. intr 21.6%, E. ovin 15%, E.pal 7.5%, E.par 18.3%. E.weyb 2.5% Al-Rubaie and Al-Saadoon (2018)
 Wasite 0–36 months 120 60 (50.0) 7 E. ahs 7.5%, E.bak 24.1%, E. cran 9.1%, E. intr 0.8%, E. ovin 18.3%, E.par 20.8%, E. weyb 5.8% Al-Saadoon and Al-Rubaie (2018)
 Kirkuk < 1 to > 2 years 160 23 (27) 8 E. bak 26%, E. cran 21.7%, E. fau 39%, E. gran 56.5%, E. intr 56.5%, E. ovin 60.8%, E.pal 73.9%, E. par 47.8% Al-Robaiee et al. (2019)
Italy
 Rome – 20 – 5 E. ahs, E. bak, E. intr, E. ovin, E. parva Battelli and Poglayen (1980)
Jordan
 Sekhra Ewes 61 39 (63.4) NS NS Jawasreh et al. (2013)
Kenya
 Different districts < 1 to > 1 years 50 NS 10 E. ahs, E. bak 43%, E. cran, E. fau, E. gran, E. intr, E. ovin 16.5%, E. pal, E. par Kanyari (1993)
 Nyandarua Different 575 253 (44.0) 8 E. ahs 15.2%, E. bak 43.6%, E. fau 2.8%, E. gran 4.8%, E. intr 8.27%, E. ovin 23.6%, E. pal 0.67%, E. par 1.06% Maingi and Munyua (1994)
 Kuwait Different 17 3 (17.5) 3 E. bak, E. cran, E. ovin Majeed et al. (2015)
Malaysia
 Perak NS 175 162 (92.5) NS NS. 175 animals were examined including 150 goats and 25 sheep Zainalabidin et al. (2015)
Mexico
 Huixquilucan Ewes, lambs 62 NS 9 E. ahs, E. bak, E. cran, E. fau, E. gran, E. intr, E. ovin, E. pal, E. par Gonzalez et al. (1990)
 Southeast region I 2 months to 2 years 412 NS 11 E. ahs, E. bak, E. cran, E. fau, E. gran, E. intr, E. mar, E. ovin, E. pal, E. par, E. weyb Trejo-Huitrón et al. (2020)
Nigeria
 Ibadan NS 1040 832 (80.0) 7 E. arloingi 10%, E. fau 31%, E. gran 3%, E. intr 6%, E. Ninakohlyakimovae 22%, E. pal 19%, E. par 8% Majaro and Dipeolu (1981)
 Gwagwalada Adult, young 44 1 (2.3) 1 E. fau Jegede et al. (2015)
Sri Lanka
 Jaffna Adults, lambs 100 76 (76.0) 4 E. bak, E. intr, E. ovin, E. par Kandasamy et al. (2011)
Sudan
 Khartoum Adult, lambs NS 58.8% 11 E. ahs 42%, E. bak 60%, E. cran 33%, E. fau 28.9%, E. gran 7.7%, E. intr 9.7%, E. mar 12.7%, E. ovin 47%, E. pal 11%, E. par 27%, E. pun 0.9% Elamin et al. (2004)
Pakistan
 Punjab More or less than 6 months 486 209 (43.0) 5 E. ahs 45.4%, E. fau 19.1%, E. intr 28.7%, E. ovin 48.3%, E. par 24.4% Khan et al. (2011)
Papua New Guinea
 University farms < 1 to > 3 years 75 67 (89.0) 8 E. ahs 45%, E. bak 72%, E. cran 39%, E. fau 28%, E. intr 24%, E. gran 4%, E. ovin 48%, E. par 58% Varghese and Yayabu (1985)
 Different regions NS 110 19 (17.3) NS NS Koinari et al. (2013)
Poland
 Various regions Adult 400 136 (34.1) NS NS Gorski et al. (2004)
 Western Pomerania NS 20 20 (100) NS NS Juszczak et al. (2019)
Saudi Arabia
 Jeddah Different 100 41 (41.0) 4 E. arloingi 22%, E. bak 17.1%, E. intr 26.8%, E. par 31.7% Toulah (2007)
 Al-Baha Different 487 227 (46.6) 8 E. ahs 12.3%, E. bak 27.9%, E. cran 29.8%, E. fau 7.6%, E. intr 9.9%, E. pal 2.9%, E. par 4.7%, E. weyb 23.4%, Ibrahim and Afsa (2013)
Scotland
 Hirta, St Kilda Lambs, adults Different Different 11 E. ahs 27. 5%, E. bak 33.7%, E. cran 22.1%, E. fau 24%, E. gran 13.3%, E. intr 28.2%, E. mar 19.8%, E. ovin 19.8%, E. pal 9.5%, E. par 27.1%, E. weyb 18.7% Craig et al. (2007)
Senegal
 Sahelian zone 6 months-4 years 2234 2204 (94.0) 8 E. ahs 28%, E. bak 69.6%, E. cran 62%, E. fau 23%, E. intr 15%, E. ovin 75.6%, E. pal 18%, E. par 25% Vercruysse (1982)
Slovakia
 Various regions Adults, lambs 445 445 (100.0) 5

E. par (in lambs 42%, in adults 37%), E. bak, E. cran, E. fau, E. ovin

2% of oocysts in lambs and 5% in adults could not be identified

 Vasilková et al. (2004)
South Africa
 North-West < 1 year NS NS 6 E. ahs 40%, E. bak 100%, E. cran 100%, E. intr 20%, E. ovin 20%, E. weyb 60% Bakunzi et al. (2010)
Spain
 Galicia Different 1882 1393 (74.0) 9 E. ahs 71%, E. bak 59%, E. cran/E. weyb 64%, E. fau 59%, %, E. gran 18%, E. intr 15%, E. mar 3%, E. ovin 74%, E. par 36% Díaz et al. (2010)
 Cartagena < 1 to > 1 year 396 396 (100.0) 11 E. ahs 75.8%, E. bak 48.5%, E. cran 89.4%, E. fau 62.1%, E. gran 74.2%, E. intr 18.2%, E. mar 43.9%, E. ovin 97%, E. par/E.pal 97%, E. weyb 90.9% Carrau et al. (2018)
Tanzania
 Vingunguti < 2 years 43 40 (93.0) 7 E. ahs 21%, E. bak 29%, E. cran 96%, E. fau 29%, E. gran 8%, E. ovin 29%, E. par 92% Kusiluka et al. (1996)
 Morogoro > 1 year 121 118 (97.5) NS NS Kambarage et al. (1996)
Turkey
 Elaziğ 2–4 months 155 147 (94.8) 9 E. ahs, E. bak, E. cran, E. ninakohlyakimovae, E. fau, E. gran, E. intr, E. pal, E. par, Güler et al. (1990)
 Different regions NS 444 434 (97.7) 9 E. ahs, 29.9%, E. bak 39.4%., E. cran 3.9%, E. fau 1.1%, E. gran 41.9%, E. intr 19.3, E. ninakohlyakimovae 16.3%, E. pal 0.4%, E. par 6.6% Demir (1995)
 Kars Different 592 556 (93.9) 10 E. ahs 23.4%, E. bak 46.6%, E. cran 13.7%, E. fau 15.1%, E. gran 27.7%, E. intr 13.9%, E. ovin 47.7%, E. pal 23.2%, E. par 37.1%, E. pun 2.3% Arslan et al. (1999)
 Van NS 350 349 (99.9) 9 E. ahs 39.4%, E. bak 39.1%, E. cran 38.8%, E. fau 15.4%, E. gran 16.5%, E. intr 11.4%, E. ovin 43.1%, E. pal 33.1%, E. par 46.5% Gül and Değer (2002)
 Antakya Lambs 248 248 (100.0) 10 E. ahs 11.3%, E. bak 38.7%, E. cran 64.9%, E. fau 11.3%, E. intr 9.3%, E. mar 16.9%, E. ovin 55.2%, E. pal 3.6%, E. par 13.3%, E. weyb 30.2% Kaya (2004)
 Bitlis NS 241 215 (89.2) 9 E. ahs 46.1%, E. bak 49.4%, E. cran 35.2%, E. fau 10.7%, E. gran 12.8%, E. intr 8.7%, E. ovin 43.5%, E. pal 30.3%, E. par 45.6%, Gül (2007)
 Van 1–60 days 132 80 (60.6) NS NS Ozdal et al. (2009)
USA
 Alabama Lambs NS NS 2 E. ahs, E. cran Smith and Davis (1961)
 Illinois NS 153 105 (69.0) 10 E. arloingi 53%, E. ahs 24%, E. cran 24%, E. fau 6%, E. gran 4%, E. intr 7%, E. ninakohlyakimovae 1%, E. pal 6%, E. par 5%, E. pun 1% Shah (1963)
 Louisiana ewes 109 94 (86.2) 10 E. ahs 41.3%, E. bak 48.6%, E. cran 36.7%, E. fau 43.1%, E. gran 28.4%, E. intr 17.4%, E. ovin 59.6%, E. pal 4.6%, E. par 45.9%, E. pun 1.8% da Silva and Miller (1991)
 Wales NS 60 57 (95.0) 9 E. ahs, E. arloingi, E. ninaekohlyakimovae, E. cran were the most common Michael and Probert (1970)
 England and Wales NS 639 NS 11 E ahs 42.1%, E bak 81.7%, E cran 71.4%, E fau 57.7%, E gran 1.7%, E intr 14.9%, E mar 14.2%,E ovin 64.8%, E pal 13.9%, E par 59.5%, E weyb 43.8%, Macrelli et al. (2019)
Zimbabwe
 Harare – 497 414 (83.3) 11 E. ahs 91%, E. bak 95%, E. caprovina 26.2%, E. christenseni 12.3%, E. cran 69.7%, E. fau 61.4%, E. gran 53.2%, E. intr 23.8%, E. ovin 100%, E. pal 24.6%, E. par 98.3% Chhabra and Pandey (1992)
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E. ahs, E. ahsata; E. bak, E. bakuensis; E. cran, E. crandallis; E. fau, E. faurei; E. gran, E. granulosa; E. intr, E. intricata; E. mar, E. marsica; E. ovin, E. ovinoidalis; E. pal, E. pallida; E. par, E. parva; E. pun, E. punctata; E. weyb, E. weybridgensis; NS, not stated. All E. ovina recorded in the table as E. bakuensis

Bold species are considered invalid

aBoth are same species but recorded with different infection rates

Eleven Eimeria spp. were detected in the present study: E. ahsata, E. bakuensis, E. crandallis, E. faurei, E. granulosa, E. intricata, E. marsica, E. ovinoidalis, E. pallida, E. parva and E. webybridgensis. These species were previously reported in sheep from Egypt (Ghanem and Abd El-Raof 2005; Abou-El-Naga 2010; Mohamaden et al. 2018); however, this is the first report of E. weybridgensis in sheep from Egypt, probably due to close similarity of their oocysts to those of E. crandallis (Norton et al. 1974). Oocysts of both species are similar shape and size. Sporocysts morphology is variable (broad ovoid 10–12 × 7–8 µm in E. crandallis and elongate ovoid 14–15 × 7–8 µm in E. weybridgensis), but not enough to easily distinguish both species (Fig. 1). Thus, both species were grouped together in our results.

In the present study, oocysts of the most pathogenic species in sheep (E. ovinoidalis) were detected in 14.6% (27/184) and all sheep were subclinical. Earlier in Egypt, subclinical E. ovinoidalis infections were also reported in 12.2% of 142 sheep from Suez governorate (Mohamaden et al. 2018). However, E. ovinoidalis and E. crandallis were detected in 13 lambs with bloody diarrhea in Kalubiya governorate (Ghanem and Abd El-Raof 2005), and respectively in 68 and 91 of 185 lambs suffered from diarrhea in Matrouh governorate (Abou-El-Naga 2010).

There is a debate concerning the validity of species of Eimeria in sheep because the endogenous stages are known only in a few of them. Some authors consider 15 Eimeria species in sheep as valid (Kaufmann 1996). Of them, 13 were reported worldwide: E. ahsata, E. bakuensis, E. crandallis, E. faurei, Eimeria gilruthi, E. granulosa, E. intricata, E. marsica, E. ovinoidalis, E. pallida, E. parva, Eimeria punctata and E. weybridgensis. In addition to Eimeria gonzalezi (Bazalar and Guerrero 1970) in sheep from South America and Eimeria dalli in Dall sheep (Ovis dalli) from Alaska, USA (Clark and Colwell 1974). Other species are considered invalid because of inadequate description or lack of archived specimens, for example Eimeria ajantai, Eimeria balloonii and Eimeria beedatus in sheep from India (More et al. 2011). Eimeria macusaniensis (camelid species) was reported in 2 sheep herds from Argentina grazed with guanaco (a closely related species to lama) on the same pasture (Vázquez et al. 2014), notable in this report, the oocyst per gram (OPG) in sheep was low (1420) in one herd; however, it exceeds 29,000 OPG in the other herd. Enteric developmental stages of E. macusaniensis were not investigated in intestinal samples of sheep. Furthermore, E. cylindrica (bovine species) infection was molecularly identified in sheep from Australia (Yang et al. 2014).

Global reports on Eimeria species infecting sheep indicating high parasite diversity in small or large scale surveys even at the level of small size populations, which revolutionize our understanding of this parasite. 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.

Acknowledgements

This study was conducted as a part of the master of the first author, and did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. We thank Dr. Ragab Fereig (South Valley University) for helping in statistical analysis.

Author’s contribution

IA, YA, MA and SA designed and coordinated the study and shared in parasite identification. EE collected and examined samples. JPD, IA and EE collected and analyzed the data, wrote and revised the manuscript.

Data availability

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

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Written informed consents were taken from owners of the sheep involved in this study prior to collection of samples.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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