Identification of the Eimeria spp. that infect Linnaeus sheep, 1758, and their morphological characteristics (Ovis aries) in Riyadh City, Saudi ArabiaABSTRACT
The epidemiology of parasitic infections in sheep is a significant problem in the fields of meat production and human health. Coccidiosis in sheep is one of the major problems caused by protozoan parasites from the genus Eimeria. This study aims to determine the prevalence of Coccidian in the Sawakni sheep breed (Linnaeus, 1758) and the epidemiology of the infection in Saudi Arabia. We used morphological characteristics to identify Eimeria spp. We collected a total of 1000 fecal samples of Ovis aries, representing different ages and genders, from cattle markets and slaughterhouses in Riyadh city. The results showed 5 species of Eimeria that infect sheep: E. ahsata (length 37±0.34 µm; width 25±0.62 µm), E. crandallis (length 22±0.81µm; width 18±0.62µm), E. marsica (length 19±0.18µm; width 12±0.56µm), E. weybridgensis (length 23±0.37µm; width 17±0.50µm), and E. ovinoidalis (length 23±0.37µm; width 17±0.50µm). Moreover, the results showed that the infection rate was 35.6%. Summer recorded the highest percentage at 46.8%, while winter recorded the lowest at 26.4%. The species Eimeria crandallis recorded the highest infection rate of 8.9%, while the species Eimeria intericata represented the lowest infection rate of 0.30%. The current study provides relevant information to assess potential infections and future defenses against sheep coccidiosis, thereby minimizing financial losses for Saudi Arabia's sheep industry.
Keywords:
sporocyst; sporozoite; sporocyst residuum; wall forming bodies; zygote
RESUMO
A epidemiologia das infecções parasitárias em ovinos é um problema significativo nas áreas de produção de carne e saúde humana. A coccidiose em ovinos é um dos principais problemas causados por parasitas protozoários do gênero Eimeria. O objetivo deste estudo é determinar a prevalência da coccidiose na raça ovina Sawakni (Linnaeus, 1758) e a epidemiologia da infecção na Arábia Saudita. Características morfológicas foram usadas para identificar Eimeria spp. Coletamos um total de 1.000 amostras fecais de Ovis aries, representando diferentes idades e gêneros, de mercados de gado e abatedouros na cidade de Riad. Os resultados mostraram 5 espécies de Eimeria que infectam ovinos: E. ahsata (comprimento 37±0,34 µm; largura 25±0,62 µm), E. crandallis (comprimento 22±0,81µm; largura 18±0,62µm), E. marsica (comprimento 19±0,18µm; largura 12±0,56µm), E. weybridgensis (comprimento 23±0,37µm; largura 17±0,50µm) e E. ovinoidalis (comprimento 23±0,37µm; largura 17±0,50µm). Além disso, os resultados mostraram que a taxa de infecção foi de 35,6%. O verão registrou a maior porcentagem, 46,8%, enquanto o inverno registrou a menor, 26,4%. A espécie Eimeria crandallis registrou a maior taxa de infecção de 8,9%, enquanto a espécie Eimeria intericata representou a menor taxa de infecção de 0,30%. O presente estudo fornece informações relevantes para avaliar possíveis infecções e futuras defesas contra a coccidiose ovina, minimizando assim as perdas financeiras para o setor ovino da Arábia Saudita.
Palavras-chave:
esporocisto; esporozoíto; resíduo de esporocisto; corpos formadores de parede; zigoto
INTRODUCTION
Sheep and goat meat are a significant part of the daily diet for people in Saudi Arabia (Abdel-Baki and Al-Quraishy, 2013; Murshed et al., 2022; Akhtar et al., 2023). Local meat production in Saudi Arabia does not meet market demand, so officials have streamlined the importation of certain sheep breeds, like the Al-Sawakni, to address the shortfall in domestic supply (Al-Owaimer et al., 2017). Al-Sawakni sheep are commonly found in southern and southeastern Africa, particularly in countries like Sudan and Ethiopia (Elrasheed et al., 2010). Coccidiosis, a global issue in sheep, is caused by the genus Eimeria, which are protozoal intracellular parasites infecting the intestinal epithelial cells (Maratea and Miller, 2007). These parasites lead to significant disease and economic losses of animal production by reducing weight gain and feed efficiency and increasing susceptibility to other diseases. Clinical coccidiosis leads to even greater financial losses for producers due to medical treatment costs, more severe impacts on growth performance, and occasional death losses. During a coccidiosis outbreak, morbidity rates can range from 10% to 40%, although mortality rarely exceeds 10% (Andrews, 2013). In most sheep production systems, nearly all animals are exposed to some species of Eimeria, though most infections remain unnoticed (Koura et al., 2001). At least 13 species of Eimeria infect sheep: Eimeria ahsata, E. bakuensis, E. crandallis, E. faurei, E. gilruthi (previously Globidium gilruthi), E. granulosa, E. intricata, E. marsica, E. ovina, E. ovinoidalis, E. pallida, E. parva, and E. weybridgensis (McDougald, 1979). Infection by Eimeria species can occur in either the small or large intestine, with the ileum, cecum, and upper colon being the most affected areas. These regions may become thickened, edematous, inflamed, and sometimes exhibit mucosal hemorrhage (Khodakaram and Mansourian, 2008). The two main pathogenic species, E. crandallis and E. ovinoidalis, have life cycles that involve parasitizing large numbers of cells during their developmental stages, leading to gradual erosion of the intestinal epithelium and, in some cases, extensive damage. This can result in secondary bacterial infections (Molina and Ruiz, 2019). Specifically, E. ahsata causes catarrhal enteritis; E. bakuensis leads to the formation of mucosal polyps; E. crandallis causes localized epithelial shedding; E. faurei also results in catarrhal enteritis; E. ovina can produce raised, visible white, opaque patches containing large numbers of oocysts in the small intestine; and E. ovinoidalis causes hemorrhagic colitis and typhlitis (Andrews, 2013). Researchers have also investigated other types of coccidiosis caused by the genus Sarcocystis in animals slaughtered in Riyadh, Saudi Arabia, and found that Al-Sawakni sheep were infected with this parasite (Al-Quraishi, 2005). However, there are no reports on Al-Sawakni sheep coccidiosis in Riyadh city. Consequently, this study aimed to survey and determine the infection rates of coccidia parasites of the genus Eimeria in the Al-Sawakni sheep breed in Riyadh.
MATERIALS AND METHODS
A total of 1000 samples of manure from Sauakni sheep were collected at a rate of 50 samples every week for 20 weeks from 1/5/2022 to 1/4/2023. Samples were handled according to the method by Upton et al., 1991, each sample was placed in a tube, and the necessary data was written on it (place and date of collection). It was transferred to the parasite laboratory at the Department of Zoology, College of Science, King Saud University (Upton et al., 1991).
Sudan exports these sheep to the Kingdom of Saudi Arabia, where consumers favor them because of their superior meat quality and large size. They have several colors, with ears hanging down and long, and the legs are long, strong, and with hooves. The body is covered with a soft woolen cover. When it is young, it has thick, long hair. Sawakni is considered a sheep with a long, thin tail, full of fat, and characterized by the presence of a clear pulp below the neck. It is fast-growing and multiplying, and most of them produce twins and can be produced at an early age (Snyman, 2014). In this study, samples of dung from Sauakni sheep (Ovis aries) were collected and examined from livestock markets, barns, grazing areas, and all slaughterhouses in the city of Riyadh, Kingdom of Saudi Arabia.
Each of the samples was examined separately to ensure its infection or non-infection by preparing a temporary dung swab from each sample and examining it microscopically. Then the samples were classified according to their infection or non-infection with the primary vesicles of coccidia parasites. Fresh oocysts were collected from the feces of the infected sheep and concentrated by the floatation technique; 2g of each sample was put into 50 mL of saturated saline. After passing the suspension through cheesecloth, it was then centrifuged at a speed of 1500rpm for 10 minutes (Long et al., 1976). To determine the sporulation time and morphology of oocysts, freshly collected non-sporulated oocysts were suspended in 2.5% (W/V) aqueous potassium dichromate, placed in Petri dishes in the air, and allowed to sporulate at room temperature (25±2°C). Periodic samples were examined under the microscope using an oil immersion objective lens, and the progress of sporulation was recorded.
Specimens were taken from all parts of the intestine sheep's intestines from the Riyadh slaughterhouse to determine the injury in parts of the intestine make histological sections, and follow up on the cycle of sexual and asexual life and histopathological changes inside the intestines of the infected host, the tissues were kept in 10% formalin immediately after removal and 48 hours of fixation; tissue slide processing was routinely done using a set of increasing alcohol concentrations, tissue sections were embedded in paraffin blocks, and sectioned by microtome at 5µm. All tissues were stained with hematoxylin and eosin, and the histopathological changes were examined under light microscopy (Levine, 1988).
The mean as the mean ± standard error of the mean (SEM) was used to express values. The statistical analysis was performed using a one-way analysis of variance (ANOVA). A p-value ≤0.05 is statistically significant.
ETHICAL ASPECTS
No animals were used, only stool samples to determine the infection. So, “This research was not submitted to the Ethics Committee on Animal Use”.
RESULTS
In this study, 1000 samples of Sauakni sheep, Ovis aries, were examined during the period 1/12/2022 to 1/4/2023, from the livestock markets and various slaughterhouses in the city of Riyadh. After examining all the study samples, infection with coccidia parasites of the genus Eimeria was recorded, where the average total infection rate was 38.10% (Fig 1), the highest infection rate was in summer at 46.8%, and the lowest infection rate was 26.4% in winter (Table 1, Fig 2). Ten different species have been identified: E. faurei, E. intricata, E. parva, E. granulose, E. pallida, E. ahsata, E. crandallis, E. marsica, E. weybridgensis, and E. ovinoidalis. Where the infection was always mixed in all infected samples, the infection with E. crandallis was recorded by 8.9%, the highest percentage of the species in the infected samples, while the infection with E. intricata by 0,30% was the lowest percentage of infection with this types Table (2).
Based on the morphometric data, ten Eimeria species were detected in the feces of the examined sheep and identified as follows:
The sporulated oocysts are ellipsoidal or ovoid and have a two-layer yellow wall. The length of these oocysts ranged from 37±0.34 (40-36) µm, while the width of the oocysts was 25±0.62 (25-27) µm, and the ratio of length to width was 1.4 (1.4-1.5) µm. When examining the sporulated oocysts, it was revealed that there is a micropyle, the presence of a micropyle cap, and the absence of oocyst residuum. It was also found that each oocyst contains four 4-sporocysts, and 2-sporozoites and has an ovoid shape, measuring 15±0.62 (15-17) µm in length and 7±0.81 (7-8) µm in width., and the aspect ratio (shape index) was 2 (2-2.15) μm. The study proved that the sporocysts do not contain a steida body and contain the sporocyst residuum, as shown in Figure 3. F.
The sporulated oocysts are ellipsoidal to ovoid with a gray wall. The length of these oocysts ranged from 22±0.81 (22-24) µm, while the width of the oocysts was 18±0.62 (17-21) µm, and the ratio of length to width was 1.22 (1.2-1.3) µm. When examining the sporulated oocysts, it was found that there was a micropyle, sometimes a micropyle cap, and sometimes a small micropyle cap, as well as the absence of oocyst residuum. It was also found that each oocyst contains four 4-sporocysts, 2-sporozoites and has an ovoid shape, measuring 10±0.75 (9-13) µm in length and 6±0.37 (6-7) µm in width., and the aspect ratio (shape index) was 1.6 (1.6-1.7) μm. The study showed that sporocysts do not contain a steida body and contain sporocyst residuum. As in Figure 3.G.
The sporulated oocysts are ovoid and have a green wall. The measurements of these oocysts range in length from 19±0.18 (20-17) μm, while the width of the oocysts is 12±0.56 (12-13) μm, and the ratio of length to width (shape index) was 1.5 (1.4-1.5) µm. When examining the sporulated oocysts, it was found that there was no micropyle, the presence of a small micropyle cap, and the absence of an oocyst residuum. It was also found that each oocyst contains four sporocysts (4-sporocysts) that are diploid (2-sporozoites) and have an ovoid shape, measuring 9±0.1 (7-11) µm in length and 5±0.13 (5-6) µm in width, and the aspect ratio (shape index) was 1.7 (1.7-1.8) μm. The study proved that the sporocysts contain the steida body as well as the sporocyst residuum, as shown in Figure 3.H.
The sporulated oocysts are ellipsoidal to ovoid and have a smooth bilayer, colorless wall, measuring 23±0.37 (21-24) µm in length, and 17±0.50 (-16)µm in width. 18 µm, and the shape index is 1.33 (1.3-1.4) µm. When examining the sporulated oocysts, the presence of a micropyle, the presence of a wide micropyle cap, and the absence of oocyst residuum It was also found that each oocyst contains four 4-sporocysts (2-sporozoites) and has an ovoid shape, measuring 11±0.1 (8-13) µm in length and 6±0.62 (6-8) µm in width., and the aspect ratio (shape index) was 1.67 (1.6-1.7) μm. The study proved that the sporocysts do not contain the steida body, as well as the sporocyst residuum, as shown in Figure 3.I. do not contain the steida body, as well as the sporocysts residuum, as shown in Figure (3. I).
The sporulated oocysts are ellipsoidal in shape and have a smooth bilayer yellow to brown wall, measuring 23±0.43 (26-21)µm in length and 20±0.31 (19-23) μm in width, and the aspect ratio (shape index) is 1.15 (1.1-1.2) μm. When examining the sporulated oocysts, it was found that there was no micropyle, no micropyle cap, and no remnants of oocyst residuum. It was also found that each vesicle contains four 4-sporocysts, and 2-sporozoites, ovoid in shape, measuring 11±0.1 (9-13) µm in length and 6±0.87 (6-8) µm in diameter. The width and the aspect ratio (shape index) were 1.61 (1.6-1.7) μm. The study proved that sprocysts do not contain a steida body and contain the remaining body. Sporocysts residuum as in Figure (3. J).
Percentage of infection with Eimeria parasite in Al-Sawakni sheep according to the seasons of the year.
The number of infections with Eimeria types and the percentage of infection with each species: E. ahsata; E. crandallis, E. marsica, E. weybridgensis, E. aovinoidalis.
Sporulated oocysts of the ten species of Eimeria collected from naturally infecting Sauakni Sheep (Ovis aries). A, E. ahsata; B, E. crandallis; C, E. marsica; D, E. weybridgensis; E, E. aovinoidalis. (IL) Inner layer, (MI) Micropyle, (MIC) Micropyle cap, (OL) Outer layer, (Pg) Polar granule, (S) Sporocyst, (SP) Sporozoite, (SR) Sporocyst residuum, and (ST) Steida body. Scale bars=10µm.
DISCUSSION
In livestock production, enteric diseases are significant as they lead to substantial economic losses due to mortality, growth retardation, and decreased feed conversion efficiency. Coccidiosis, caused by Eimeria species, is a parasitic disease with high morbidity that impacts various animal species, including sheep. In sheep, eleven Eimeria species have been identified, primarily through microscopic examination of oocysts (Kawahara et al. 2010). Due to the pathogenic significance of Eimeria parasites, several survey studies have been conducted in the Kingdom of Saudi Arabia on Eimeria infections in local sheep. These studies did not specify the breeds of the sheep involved (Kasim and Al-Shawa, 1985; Toulah, 2007). The Eimeria species were identified as E. ahsata, E. crandallis, E. marsica, E. weybridgensis, and E. ovinoidalis. As for the first type, the parasite Eimeria ahsata was described for the first time by Honess (1942) in sheep in Italy, and in this current study it was proven that Al-Sawakni sheep in the city of Riyadh in the Kingdom of Saudi Arabia were infected with this parasite. The researcher (Hasan and Abed, 2012) re-described the parasite E. ahsata in the sheep of the city of Mosul in Iraq. And when comparing the results of this study with the results of each of the researchers (Honess, 1942) and (Hasan and Abed, 2012) in Table 2. Some minor differences were found in the sizes of the oocyst in the study (Hasan and Abed, 2012) with the current study. The second type, Eimeria crandallis, was described for the first time in sheep in Italy (Honess, 1942), and in this current study, it was proven that Al-Sawakni sheep were infected with this parasite. Our results are consistent with many studies that described the parasite E. crandallis in sheep in Germany and examined the pathogenesis of this type of parasite in Table 2 (Dittmar, 2010). As for the third type, the Eimeria marsica parasite was described for the first time in sheep in Spain (Restani, 1971), and in this current study, it was proven that the Sawakni sheep were infected with this parasite. When comparing the results of this study with the results of each of the researchers (Dittmar, 2010) and (Restani, 1971), Table 2. Some minor differences in the sizes of the oocyst were found in the study (Dittmar, 2010) and our current study with the study (Restani, 1971). The reason for the difference is due to the lack of a range of measurements by the researcher (Restani, 1971). The fourth type, Eimeria weybridgensis, was described for the first time in domestic sheep in the United Kingdom (Norton et al., 1974). The researcher (Dittmar, 2010) re-described the parasite E. weybridgensis in sheep in Germany. When comparing the results of this study with the results of each of the researchers (Dittmar, 2010), and Norton et al., 1974) in Table 2. Some slight differences in the sizes of the oocyst were found in the current study and (Dittmar, 2010) in a study (Norton et al., 1974). As for the fifth type, the parasite Eimeria ovinoidalis was described for the first time in sheep (McDougald, 1979), and in this current study, it was proven that the Sawakni sheep were infected with this parasite. The researchers re-described the parasite E. ovinoidalis in sheep in Germany and Iraq (Dittmar, 2010; Hasan and Abed, 2012), and this matches our results for the E. ovinoidalis parasite in Table 2.
The current study recorded a total infection rate with Eimeria parasites that reached 35.6% in the Sawakni sheep in the city of Riyadh, where the highest infection rate was in summer at 46.8% and the lowest infection rate in winter was 26.4%, where the infection was mixed with more than one type of Eimeria in all infected samples. In study (Toulah, 2007) on sheep in the city of Jeddah, 100 samples were collected, and the infection rate with these parasites was 41%. Four different types of parasites of the genus Eimeria were identified, where the type Eimeria parva recorded the highest infection rate of 31.7%, while Eimeria ovina recorded the lowest infection rate of 17.7%. Hence, it is clear that the current study recorded a lower total infection rate than the infection rates in previously recorded studies. The reason may be due to the nature of animal husbandry as well as to the size of the dose and the type of parasite egg sacs taken by the animals during feeding, and this is consistent with what was indicated (Levine, 1985). The number of egg sacs expelled with the feces depends on the size of the dose taken by the infected animal and on its immunity and age. It was noted in this study that there is a decrease in the infection rate in the winter season, and the temperature may reach below zero degrees Celsius at times, in contrast to the summer, which makes the sporulation process impossible on the ground (Parker and Jones 1990).
CONCLUSIONS
The presence of five Eimeria species that infect sheep has been proven and has been identified morphologically in Riyadh City. It would help in figuring out the risk of infection and give important information for figuring out how well future efforts to control coccidiosis in sheep will work. This would contribute to cut down on economic losses in sheep breeding and keep the quality of meat production high.
ACKNOWLEDGMENTS
Thanks for the Ongoing Research Funding Program No.ORF-2025-1081, at King Saud University. Also, Researchers Supporting Project No. (PNURSP2025R401), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.
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