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. 2024 May 27:11:1373842.
doi: 10.3389/fvets.2024.1373842. eCollection 2024.

Microscopic and molecular detection of piroplasms among sheep in Upper Egypt

Ahmed Kamal Dyab #  1   2 , Sara Abdel-Aal Mohamed #  3 , Fatma Mohamed Abdel-Aziz  3 , Ahmed Gareh  4 , Fathy Osman  5 , Fatma A Elgohary  6 , Ehssan Ahmed Hassan  7   8 , Noorah Alsowayeh  9 , Hind Alzaylaee  10 , Abd Al-Rahman S Ahmed  11 , Daniel Bravo-Barriga  12 , Ehab Kotb Elmahallawy  12   13
Affiliations

Microscopic and molecular detection of piroplasms among sheep in Upper Egypt

Ahmed Kamal Dyab et al. Front Vet Sci. .

Abstract

Introduction: Blood parasites pose a significant threat to livestock production in southern Egypt, yet there is a scarcity of information regarding their circulation and epidemiology in sheep in this region. This study aimed to investigate the seroprevalence of blood parasite infections in sheep in Assiut governorate, Upper Egypt.

Methods: A total of 400 blood samples were collected from sheep of varying ages and genders. The preliminary screening for the presence of piroplasms, mainly Babesia and Theileria spp., via microscopic examination, followed by investigation of the potential risk factors linked with the exposure to infection. Moreover, molecular identification of both parasites on some of positive samples was performed using PCR targeting Babesia 18S rRNA and Theileria annulata Tams1 gene.

Results: The microscopic examination revealed that among the examined sheep, there was an overall prevalence of blood parasites at 44% (176 out of 400), with Babesia spp. observed in 14% (56 out of 400) and Theileria spp. in 30% (120 out of 400). Furthermore, the infection rate was non-significantly higher in young animals (50%) compared to adults (38.5%) (P = 0.246). Male sheep exhibited a significantly higher vulnerability to both parasites' infection (63.3%) compared to females (35.7%) (P = 0.011). Interestingly, the prevalence of both blood parasites was significantly higher during the cold season (66.1%) compared to the hot season (15.9%) (P = < 0.001). The molecular analysis identified the presence of Babesia ovis and Theileria annulata among a subsample of the positive sheep's bloods films. The identified species were recorded in the GenBank™ databases and assigned specific accession numbers (OQ360720 and OQ360719 for B. ovis), and (OP991838 for T. annulata).

Conclusions: Taken together, this study confirms a high prevalence of piroplasmosis and offers epidemiological and molecular insights into blood parasites in sheep from Upper Egypt, highlighting the importance of detecting these parasites in various hosts and their competent vectors (ticks).

Keywords: Babesia; Egypt; Theileria; microscopic; molecular; piroplasm; prevalence; sheep.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer MR declared a shared affiliation with the author FE to the handling editor at the time of review.

Figures

Figure 1
Figure 1
A map illustrating the geographic region being investigated.
Figure 2
Figure 2
Thin blood film stained with Giemsa magnified × 100 (oil immersion lens) showing the blood protozoan parasites found in sheep (A, B): paired Trophozoites of Babesia spp. (arrow).
Figure 3
Figure 3
(A) Echincyte containing trophozoites of Theileria spp., x100 (oil immersion lens), (B) ring stage of Theileria spp., x100 (oil immersion lens), (C) multiple microshizonts of Theileria spp. x100 (oil immersion lens) (arrow), (D) small rod shape trophozoite of Theileria spp., x100 (oil immersion lens) (thin arrow), rounded shape trophozoite of Theileria spp., x 100 (oil immersion lens) (thick arrow).
Figure 4
Figure 4
Phylogenetic relationships of Babesia ovis were inferred based on the analysis of 40 nucleotide 18S rRNA gene sequences using the Maximum Likelihood method and Kimura 2-parameter model. The tree with the highest log likelihood (−1656.70) is shown. A discrete Gamma distribution was used to model evolutionary rate differences among sites [5 categories (+G, parameter = 0.3354)]. The rate variation model allowed for some sites to be evolutionarily invariable ([+I], 51.51% sites). Bootstrap values >75% in 1000 repetitions are indicated at specific branch nodes. The bar indicates the average number of substitutions per site. The tree was rooted using Theileria annulata (KT367871) as the outgroup. Sequences obtained during this study are shown in boldface.
Figure 5
Figure 5
A circular phylogenetic tree of Theileria annulata based on the analysis of 24 nucleotide tams1 gene sequences using the Maximum Likelihood method and the Tamura 3-parameter model. The tree depicts the highest log likelihood (−10113.12). Evolutionary rate differences among sites were modeled using a discrete Gamma distribution with 5 categories (+G, parameter = 0.4271). Bootstrap values greater than 75% in 1000 repetitions are indicated at specific branch nodes. The bar represents the average number of substitutions per site. Sequences obtained during this study are highlighted in boldface.
Figure 6
Figure 6
The percentages of identity for the studied isolates of B. ovis in sheep related to other isolates worldwide depend on B. ovis 18S rRNA gene.
Figure 7
Figure 7
The percentages of identity for the studied isolates of Theileria annulata in sheep related to other isolates worldwide depend on Theileria annulata tams1 gene.
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