Skip to main content
Log in

Morphologic and molecular identification of three macroscopic Sarcocystis species infecting domestic sheep (Ovis aries) and cattle (Bos taurus) in Egypt

  • Protozoology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In a survey study on the macroscopic species of Sarcocystis infecting domestic sheep (Ovis aries) and cattle (Bos taurus) in Egypt, the macrosarcocysts of Sarcocystis gigantea and Sarcocystis medusiformis were detected in the carcasses of 33 domestic sheep out of a total of 250 (13.20%), whereas Sarcocystis hirsuta macrosarcocysts were found in 17 out of 150 cattle (11.33%) slaughtered at the municipal abattoirs of two different provinces in Egypt. The sarcocysts of each species were thoroughly described morphologically through gross inspection, histopathologic and transmission electron microscopic (TEM) examination. By TEM, S. gigantea primary cyst wall was 6–7.5 μm thick and had irregular highly branched cauliflower-like villar protrusions (VP).The VP contained microtubules (mt) and multiple electron dense granules (edg) that were dispersed inside the cores of the branched VP. Besides, the parasitophorous vacuolar membrane (PVM) had minute blister-like invaginations all over the entire surface of the sarcocyst. S. medusiformis cyst had a thin sarcocyst wall (~2 μm thick) as compared to that of S. gigantea. The cyst wall had trapezoidal or nearly pyramidal VP that were surrounded by thick PVM in addition to a ground substance GS that contained electron-dense fine particles. S. hirsuta sarcocyst wall was 7–9 μm thick and possessed rhomboid-shaped VP that contained microtubules (mt) and electron-dense granules (edg) of variable sizes. The edg were arranged in rows and running parallel to the longitudinal axis of the protrusions. The VP had characteristic narrow neck-like constrictions at their bases, dilated middle portions, and tapered distal ends. The detected macrosarcocysts were eventually confirmed by molecular characterization on the levels of 18S rRNA, 28S rRNA, and Cox1 sequences. Phylogenetic analyses based on the sequences of the 18S rRNA and Cox1 genetic markers gave rise to robust associations of the currently identified isolates of S. gigantea, S. medusiformis, and S. hirsuta within a major clade of Sarcocystis species with felines as presumed or known definitive hosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ahmed AM, Elshraway NT, Youssef AI (2016) Survey on Sarcocystis in bovine carcasses slaughtered at the municipal abattoir of El-Kharga, Egypt, Veterinary World, 9(12): 1461-1465. doi: https://doi.org/10.14202/vetworld.2016.1461-1465

  • Bahari P, Salehi M, Seyedabadi M, Mohammadi A (2014) Molecular identification of macroscopic and microscopic cysts of Sarcocystis in sheep in North Khorasan Province, Iranian International Journal of Molecular and Cellular Medicine. Winter 3(1), 51–56

  • Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271

    Article  CAS  Google Scholar 

  • Bittencourt MV, Meneses IDS, Ribeiro-Andrade M, de Jesus RF, de Araújo FR, Gondim LFP (2016) Sarcocystis spp. in sheep and goats: frequency of infection and species identification by morphological, ultrastructural, and molecular tests in Bahia, Brazil. Parasitol Res 115:1683–1689

    Article  Google Scholar 

  • Bottner A, Charleston WAG, Hopcroft D (1987a) The structure and identity of macroscopically visible Sarcocystis cysts in cattle. Vet Parasitol 24:35–45

    Article  CAS  Google Scholar 

  • Bottner A, Charleston WAG, Pomroy WE, Rommel M (1987b) The prevalence and identity of Sarcocystis in beef cattle in New Zealand. Vet Parasitol 24:157–168

    Article  CAS  Google Scholar 

  • Collins GH, Charleston WAG, Moriarty KM (1976) Sarcocystis species in sheep [Letters to the editor]. N Z Vet J 24:123–124. https://doi.org/10.1080/00480169.1976.34299

  • Collins GH, Atkinson E, Charleston WAG (1979) Studies on Sarcocystis species. III: the macrocystic species of sheep. N Z Vet J 27:204–206. https://doi.org/10.1080/00480169.1979.34651

    Article  CAS  PubMed  Google Scholar 

  • Dubey JP, Odening K (2001) Toxoplasmosis and related infections. In: Samuel WM, Pybus MJ, Kocan AA (eds) Parasitic diseases of wild mammals. Iowa State University Press, Ames, Iowa, pp 478–519

    Chapter  Google Scholar 

  • Dubey JP, Speer CA, Charleston WAG (1989) Ultrastructural differentiation between sarcocysts of Sarcocystis hirsuta and Sarcocystis hominis. Vet Parasitol 34:153–157

    Article  CAS  Google Scholar 

  • Dubey JP, Moré G, van Wilpe E, Calero-Bernal R, Verma SK, Schares G (2015) Sarcocystis rommeli, n. sp. (Apicomplexa: Sarcocystidae) from cattle (Bos taurus) and its differentiation from Sarcocystis hominis. J Eukaryot Microbiol 63:62–68. https://doi.org/10.1111/jeu.12248

    Article  PubMed  Google Scholar 

  • Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R (2016) Sarcocystosis of animals and humans, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Ellis TJ, Luton K, Baverstock PR, Whitworth G, Tenter AM, Johnson AM (1995) Phylogenetic relationships between Toxoplasma and Sarcocystis deduced from a comparison of 18S rDNA sequences. Parasitology 110 (Pt 5), 5 21–528

  • El-Morsey A, El-Seify M, Desouky AY, Abdel-Aziz MM, Sakai H, Yanai T (2014) Morphologic identification of a new Sarcocystis sp. in the common moorhen (Gallinula chloropus) (Aves: Gruiformes: Rallidae) from Brolos Lake, Egypt. Parasitol. Res. 113:391–397. https://doi.org/10.1007/s00436-013-3667-x

  • El-Morsey A, El-Seify M, Desouky AR, Abdel-Aziz MM, El-Dakhly KM, Kasem S, Abdo W, Haridy M, Sakai H, Yanai T (2015a) Morphologic and molecular characteristics of Sarcocystis atraii n. sp. (Apicomplexa: Sarcocystidae) infecting the common coot (Fulica atra) from Egypt. Acta Parasitol 60:691–699. https://doi.org/10.1515/ap-2015-0098

    Article  PubMed  Google Scholar 

  • El-Morsey A, El-Seify M, Desouky AY, Abdel-Aziz MM, Sakai H, Yanai T (2015b) Sarcocystis chloropusae (protozoa: Sarcocystidae) n. sp. from the common moorhen (Gallinula chloropus) from Egypt. Parasitology 142:1063–1065. https://doi.org/10.1017/s0031182015000293

  • El-Morsey A, Abdo W, Sultan K, Elhawary NM, Abou Zaid AA (2019) Ultrastructural and molecular identification of the sarcocysts of Sarcocystis tenella and Sarcocystis arieticanis infecting domestic sheep (Ovis aries) from Egypt. Acta Parasitol 64:501–513

    Article  CAS  Google Scholar 

  • El-Seify M, El-Morsey A, Hilali M, Zayed A, El-Dakhly K, Haridy M, Sakai H, Yanai T (2014) Molecular characterization of Sarcocystis fusiformis and Sarcocystis buffalonis infecting water buffaloes (Bubalus bubalis) from Egypt. Am J Anim Vet Sci 9:95–104. https://doi.org/10.3844/ajavssp.2014.95.104

    Article  CAS  Google Scholar 

  • Fischer S, Odening K (1998) Characterization of bovine Sarcocystis species by analysis of their 18S ribosomal DNA sequences. J Parasitol 84:50–54. https://doi.org/10.2307/3284529

    Article  CAS  PubMed  Google Scholar 

  • Gjerde B (2013) Phylogenetic relationships among Sarcocystis species in cervids, cattle and sheep inferred from the mitochondrial cytochrome c oxidase subunit I gene. Int J Parasitol 43:579–591. https://doi.org/10.1016/j.ijpara.2013.02.004

    Article  CAS  PubMed  Google Scholar 

  • Gjerde B (2014a) Morphological and molecular characteristics of four Sarcocystis spp. in Canadian moose (Alces alces), including Sarcocystis taeniata n. sp. Parasitol Res 113:1591–1604

    Article  Google Scholar 

  • Gjerde B (2014b) Sarcocystis species in red deer revisited: with a redescription of two known species as Sarcocystis elongata n. sp. and Sarcocystis truncata n. sp. based on mitochondrial cox1 sequences. Parasitology 141:441–452

    Article  Google Scholar 

  • Gjerde B (2016) Molecular characterisation of Sarcocystis bovifelis, Sarcocystis bovini n. sp., Sarcocystis hirsuta and Sarcocystis cruzi from cattle (Bos taurus) and Sarcocystis sinensis from water buffaloes (Bubalus bubalis) Parasitol. Res. 115:1473–1492. https://doi.org/10.1007/s00436-015-4881-5

    Article  Google Scholar 

  • Gjerde B, Josefsen TD (2015) Molecular characterisation of Sarcocystis lutrae n. sp. and Toxoplasma gondii from the musculature of two Eurasian otters (Lutra lutra) in Norway. Parasitol Res 114:873–886. https://doi.org/10.1007/s00436-014-4251-8

    Article  PubMed  Google Scholar 

  • Gjerde B, Schulze J (2014) Muscular sarcocystosis in two arctic foxes (Vulpes lagopus) due to Sarcocystis arctica n. sp.: sarcocyst morphology, molecular characteristics and phylogeny. Parasitol Res 113:811–821. https://doi.org/10.1007/s00436-013-3711-x

    Article  PubMed  Google Scholar 

  • Gjerde B, de la Fuente C, Alunda JM, Luzón M (2020) Molecular characterisation of five Sarcocystis species in domestic sheep (Ovis aries) from Spain. 119: 215-231. https://doi.org/10.1007/s00436-019-06504-6

  • Gual I, Bartley PM, Katzer F, Innes EA, Canton GJ, Moore DP (2017) Molecular confirmation of Sarcocystis gigantea in a naturally infected sheep in Argentina: a case report. Vet Parasito 248:25–27

    Article  Google Scholar 

  • Hilali M, El-Seify M, Zayed A, El-Morsey A, Dubey JP (2011) Sarcocystis dubeyi (Huong and Uggla 1999) infection in water buffaloes (Bubalus bubalis) from Egypt. J Parasitol 97:527–528. https://doi.org/10.1645/GE-2656.1

    Article  CAS  PubMed  Google Scholar 

  • Hu JJ, Huang S, Wen T, Esch GW, Liang Y, Li HL (2017) Sarcocystis spp. in domestic sheep in Kunming City, China: prevalence, morphology, and molecular characteristics. Parasite 24:30. https://doi.org/10.1051/parasite/2017025

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeffries AC, Schnitzler B, Heydorn AO, Johnson AM, Tenter AM (1997) Identification of synapomorphic characters in the genus Sarcocystis based on 18S rDNA sequence comparison. J Eukaryot Microbiol 44(5):388–392

    Article  CAS  Google Scholar 

  • Kalantari N, Khaksar M, Ghaffari S, Hamidekish SM (2016) Molecular analysis of Sarcocystis spp. isolated from sheep (Ovis aries) in Babol Area, Mazandaran Province, Northern Iran. Iranian Journal of Parasitology 11(1):73–80

    PubMed  PubMed Central  Google Scholar 

  • Kolenda R, Schierack P, Zieba F, Zwijacz-Kozica T, BednarskiM (2015) Firstmolecular characterization of Sarcocystis tenella in Tatra chamois (Rupicapra rupicapra tatrica) in Poland. Parasitol Res 114: 3885–3892. https://doi.org/10.1007/s00436-015-4619-4

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  Google Scholar 

  • Mahran OM (2009) Sarcocystis infection in sheep and goats slaughtered in Shalatin abattoir, Red Sea Governorate, Egypt. Assiut Veterinary Medical Journal 55(121):1–15

    Google Scholar 

  • Martínez-Navalón B, Anastasio-Giner B, Cano-Fructuoso M, Sánchez-Martínez P, Llopis-Morant A, Pérez-Castarlenas B, Goyena E, Berriatua E (2012) Short communication. Sarcocystis infection: a major cause of carcass condemnation in adult sheep in Spain. Span J Agric Res 10:388–392. https://doi.org/10.5424/sjar/2012102-523-11

    Article  Google Scholar 

  • Mugridge NB, Morrison DA, Heckeroth AR, Johnson AM, Tenter AM (1999) Phylogenetic analysis based on full-length large subunit ribosomal RNA gene sequence comparison reveals that Neospora caninum is more closely related to Hammondia heydorni than to Toxoplasma gondii. Int J Parasitol 29:1545–1556

    Article  CAS  Google Scholar 

  • Mugridge NB, Morrison DA, Jakel T, Heckeroth AR, Tenter AM, Johnson AM (2000) Effects of sequence alignment and structural domains of ribosomal DNA on phylogeny reconstruction for the protozoan family Sarcocystidae Molecular Biology and Evolution. 17 (12), 1842–1853

  • Munday BL, Obendorf DL (1984) Morphology of Sarcocystis gigantea in experimentally-infected sheep. Vet Parasitol 16:193–199. https://doi.org/10.1016/0304-4017(84)90036-0

    Article  CAS  PubMed  Google Scholar 

  • Nahed H, Ghoneim WM, Reda W, Nader MS (2014) Occurrence of zoonotic sarcosporidiosis in slaughtered cattle and buffaloes in different abattoirs in Egypt. Global Veterinaria 13 (5): 809-813. doi;https://doi.org/10.5829/idosi.gv.2014.13.05.86211

  • O’Donoghue PJ, Ford GE (1986) The prevalence and intensity of Sarcocystis spp. infections in sheep. Aust Vet J 63:273–278

    Article  Google Scholar 

  • Obendorf DL, Munday BL (1987) Experimental infection with Sarcocystis medusiformis in sheep. Vet Parasitol 24:59–65. https://doi.org/10.1016/0304-4017(87)90130-0

    Article  CAS  PubMed  Google Scholar 

  • Oryan A, Moghaddar N, Gaur SNS (1996). The distribution pattern of Sarcocystis species, their transmission and pathogenesis in sheep in Fars province of Iran. Vet. Res. Com. 20, 243–253. S0031 18201 30018 19

  • Pipia AP, Varcasia A, Zidda A, Dessì G, Panzalis R, Tamponi C, Marrosu R, Tosciri G, Sanna G, Dore F, Chiesa F, Scala A (2016) Crosssectional investigation on sheep sarcosporidiosis in Sardinia, Italy. Veterinary Parasitology Regional Studies and Reports 3–4:13–17. https://doi.org/10.1016/j.vprsr.2016.05.004

    Article  Google Scholar 

  • Prakas P, Butkauskas D, Rudaitytė E, Kutkienė L, Sruoga A, Pūraitė I (2016) Morphological and molecular characterization of Sarcocystis taeniata and Sarcocystis pilosa n. sp from the sika deer (Cervus nippon) in Lithuania. Parasitol Res 115:3021–3032. https://doi.org/10.1007/s00436-016-5057-7

    Article  PubMed  Google Scholar 

  • Prakas P, Rudaitytė E, Butkauskas D, Kutkienė L (2017) Sarcocystis entzerothi n. sp. from the European roe deer (Capreolus capreolus). Parasitol Res 116:271–279. https://doi.org/10.1007/s00436-016-5288-7

    Article  PubMed  Google Scholar 

  • Prakas P, Kirillova V, Calero-Bernal R, Kirjušina M, Rudaityte-Lukošiene E, Habela MÁ, Gavarane I, Butkauskas D (2019) Sarcocystis species identification in the moose (Alces alces) from the Baltic States. Parasitol Res 118:1601–1608. https://doi.org/10.1007/s00436-019-06291-0

    Article  PubMed  Google Scholar 

  • Sayed FG, Shaheen MSI, Arafa MI, Koraa HM (2008) Sarcocystis infection in cattle at Assiut abattoir: microscopical and serological studies. Assiut University Bulletin of Research 11:47–57

    Google Scholar 

  • Shekarforoush SS, Razavi SM, Abbasvali M (2013) First detection of Sarcocystis hirsuta from cattle in Iran. Ir. J. Vet. Res.14:155–157

  • Smith AF, Semeniuk CA, Kutz SJ, Massolo A (2014) Dog-walking behaviours affect gastrointestinal parasitism in park-attending dogs. Parasites and Vectors 7:429. https://doi.org/10.1186/1756-3305-7-429

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Ahmed El-Morsey conceptualized and designed the study, collected samples, morphologic and molecular diagnosis of the three Sarcocystis species, analyzed data, and wrote the manuscript. Wlied abdo performed the histopathology and assisted in data analysis and diagnosis. Attia A. Abou Zaid and Shimaa S.GH. Sorour collected samples and assisted in study design, survey data collection, and identification of Sarcocystis species.

Corresponding author

Correspondence to Ahmed El-Morsey.

Ethics declarations

The muscle specimens used in the current study were collected from sheep and cattle carcasses according to local standard regulations and laws of the two abattoirs in El-Mahalla El-Kobra and Sedi-Salem cities belonging to Gharbia and Kafr El-Sheikh provinces, respectively, Egypt.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Section Editor: Daniel K Howe

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El-Morsey, A., Abdo, W., Zaid, A.A.A. et al. Morphologic and molecular identification of three macroscopic Sarcocystis species infecting domestic sheep (Ovis aries) and cattle (Bos taurus) in Egypt. Parasitol Res 120, 637–654 (2021). https://doi.org/10.1007/s00436-020-07002-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-07002-w

Keywords

Navigation