Meat sarcocystosis: a critical meat-borne parasite impacting carcasses in abattoirs

Main Article Content

Nady Elbarbary https://orcid.org/0009-0006-5521-6310
Mounir M. Bekhit
Ahmed Garh
Ahmed Fotouh
Mohamed K. Dandrawy
Wageh S. Darwish
Neveen M. Abdelmotilib
Marwa A. Ali
Mohamed M. Salem
Maha Abdelhaseib

Keywords

abattoirs, meat, postmortem inspection, PCR-RFLP, Sarcocystis

Abstract

One of the most commonly occurring foodborne, tissue cyst-forming protozoan zoonotic parasites with public health and veterinary relevance is Sarcocystis species. This research was conducted using traditional and molecular techniques to identify the incidence of Sarcocystis spp. in 750 slaughtered bovine animals of varying age and sex (375 cattle and 375 buffalo) at various abattoirs in Aswan Governorate, Egypt. The overall occurrence of macroscopic lesions of Sarcocystis spp. in cattle and buffaloes was 20.5% and 38.4%, respectively, while the occurrence of microscopic infection was 30.4% and 70.1%, respectively. Furthermore, the disease strongly correlated with the measured variables, such as the animal’s age and sex. Animals older than 5 years had the highest infection rate, and females had higher infection rates than males. The esophagus, tongue, and diaphragm had the highest rates of sarcocyst compared to other organs. Histopathology studies of sarcocyst in various tissues revealed encased, circular to elongated, basophilic sarcocysts with numerous bradyzoites embedded in muscle fibers. PCR-RFLP reports that S. cruzi, S. hominis, S. hirsuta, S. buffalonis, and S. fusiformis were the species most often found. Moreover, such frequency highlights the pressing need for an effective disease control strategy and a systematic surveillance system among bovine populations. We strongly encourage the One Health approach to reduce zoonotic spread to humans and financial losses in the livestock industry.

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References

Ahmed A. M., Elshraway N. T. & Youssef A. (2016). Survey on Sarcocystis in bovine carcasses slaughtered at the municipal abattoir of El-Kharga, Egypt, Veterinary World, 9, 1461- 1465. https://doi.org/10.14202/vetworld.2016.1461-1465
Albayati H. H., and Jassem G. A. (2023). Traditional, histopathological and molecular diagnosis of sarcocytosis in slaughtered sheep in Al-Diwaniyah province, Iraq. Iraqi Journal of Veterinary Sciences, 37, 871-875. https://doi.org/10.33899/ijvs.2023.138763.2835
Ayazian M. S., Teimouri A., Mohebali M., Sharifi Yazdi M. K., Shojaee S., Rezaian M. (2020). Sarcocystis infection in beef and industrial raw beef burgers from butcheries and retail stores: a molecular microscopic study. Heliyon, 6, e04171. https://doi.org/10.1016/j.heliyon.2020.e04171
Branger B. (2013). Valeur diagnostique et prédictive d’un test de diagnostic ou de dépistage. 11. In: Test Diagnostique. Réseau de Périnatalité des Pays de la Loire. Nantes, France. Available from: https://www.reseau-naissance.fr/data/mediashare/zy/5lort-2g2ifme9q429gvnfgmoh0xctd-rg.pdf
Bucca M., Brianti E., Giuffrida A., Ziino G., Cicciari S., & Panebianco A. (2011). Prevalence and distribution of Sarcocystis spp. cysts in several muscles of cattle slaughtered in Sicily, Southern Italy. Food Control, 22, 105-108. https://doi.org/10.1016/j.foodcont.2010.05.015
Centers for Disease Control and Prevention (CDC). (2000). Surveillance for foodborne-disease outbreaks-United States, 1993-1997. Morbidity and Mortality Weekly Report, 49, 1-62
Chauhan R. S. & Agarwal D. K. (2008). Textbook of Veterinary, Clinical and Laboratory Diagnosis (2nd ed.). Jaypee Brothers Medical Publishers, New Delhi, India (pp. 1–364).
Chiesa F., Muratore E., Dalmasso A., & Civera T. (2013). A new molecular approach to assess the occurrence of Sarcocystis spp. in cattle and products thereof: preliminary data. Italian Journal of Food Safety, 2, 148-151. https://doi.org/10.4081/ijfs.2013.1580
Dafedar A., D’Souza P. E., & Mamatha G. S. (2011). Prevalence and morphological studies on Sarcocystis species infecting cattle in Bangalore. Journal of Veterinary Parasitology, 25, 183-184.
Dalir Ghaffari A., Dalimi A., & Pirestani M. (2022). Microscopic and Molecular Detection of Sarcocystis cruzi (Apicomplexa: Sarcocystidae) in the Heart Muscle of Cattle. Iranian Journal of Parasitology, 17, 535–542. https://doi.org/10.18502/ijpa.v17i4.11281
Dong H., Su R., Wang Y., Tong Z., Zhang L., Yang Y., & Hu J. (2018). Sarcocystis species in wild and domestic sheep (Ovis ammon and Ovis aries) from China. BMC Veterinary Research, 14, 377. https://doi.org/10.1186/s12917-018-1712-9
Dubey J. P. (2015). Foodborne and waterborne zoonotic sarcocystosis. Food Waterborne Parasitology, 1, 2-11. https://doi.org/10.1016/j.fawpar.2015.09.001
Elbarbary N. K., Darwish W. S., Fotouh A., & Mohamed K. D. (2024). Unveiling the mix-up: investigating species and unauthorized tissues in beef-based meat products. BMC Veterinary Research, 20, 380 . https://doi.org/10.1186/s12917-024-04223-4
El-Kady A. M., Hussein N. M., & Hassan A. A. (2018). First molecular characterization of Sarcocystis spp. in cattle in Qena Governorate, Upper Egypt. Journal of Parasitic Diseases, 42, 114- 121. https://doi.org/101007/s12639-017-0974-7
Elrais A., Reda A. G., Abo-Bakr M. E., & Hanan M. L. (2022). Prevalence and distribution patterns of Sarcocysts in cattle carcasses slaughtered at the municipal abattoir of Tanta, Egypt. Benha Veterinary Medical Journal, 42, 194-197. https://doi.org/10.21608/bvmj.2022.131800.1511
El-Sayad M., El-Taweel H., Ahmed A., & Abd El-Latif N. (2023). Sarcocystosis among buffaloes from slaughterhouses in Nile Delta, Egypt: morphologic assessment and molecular confirmation. Iranian Journal of Veterinary Research, 24, 313-319. https://doi.org/10.22099/IJVR.2023.48129.7006
Elshahawy I. S., Mohammed E., Gomaa A., & Fawaz M. (2022). Sarcocystiscruzi in Egyptian slaughtered cattle (Bos taurus): epidemiology, morphology and molecular description of the findings. Iranian Journal of Veterinary Research, 23, 337–348. https://doi.org/10.22099/IJVR.2022.43498.6363
FAO/WHO. (2014). Multicriteria-based ranking for risk management of food-borne parasites. Microbiological Risk Assessment Series No. 23 (pp. 302). Rome. E-ISBN 978-92-5-108200-3 https://www.who.int/foodsafety/publications/mra _23
Fayer R., Esposito D. H., & Dubey J. P. (2015). Human infections with Sarcocystis species. Clinical Microbiology Reviews, 28, 295-311. https://doi.org/10.1128/CMR.00113-14
Ferreira M. S., Vogel F. S., Sangioni L. A., Cezar A.S., Braunig P., de Avilla Botton S., Camillo G., & Portella L. P. (2018). Sarcocystis species identification in cattle hearts destined to human consumption in southern Brazil. Veterinary Parasitology: Regional Studies and Reports, 14, 94-98. https://doi.org/10.1016/j.vprsr.2018.09.002
Fotouh A., Shosha E. A., Zanaty A. M., & Darwesh M. M. (2024). Immunopathological investigation and genetic evolution of Avian leukosis virus Subgroup-J associated with myelocytomatosis in broiler flocks in Egypt. Virology Journal, 21, 83. https://doi.org/10.1186/s12985-024-02329-7
Gareh A., Soliman M., Saleh A. A., El-Gohary F. A., El-Sherbiny H. M., Mohamed R. H., & Elmahallawy E. K. (2020). Epidemiological and Histopathological Investigation of Sarcocystis spp. in Slaughtered Dromedary Camels (Camelus dromedarius) in Egypt. Veterinary Sciences, 7, 162. https://doi.org/10.3390/vetsci7040162
Gjerde B., Hilali M., & Abbas I. E. (2016). Molecular differentiation of Sarcocystis buffalonis and Sarcocystis levinei in water buffaloes (Bubalus bubalis) from Sarcocystis hirsuta and Sarcocystis cruzi in cattle (Bos taurus). Parasite Research, 115(6), 2459-2471. https://doi.org/10.1007/s00436-016-4998-1
GOVS, 1986. General Organization for Veterinary Services, Law (517).
Gupta A., de Araujo L.S., Hemphill A., Asis K, Benjamin M. R., & Jitender P. D. (2024). Morphological and molecular characterization of a Sarcocystis bovifelis-like sarcocyst in American beef. Parasites Vectors, 17, 543. https://doi.org/10.1186/s13071-024-06628-4
Hajimohammadi B., Dehghani A., Moghadam Ahmadi M., Eslami G., Oryan A., & Khamesipour A. (2014). Prevalence and species identification of Sarcocystis in raw hamburgers distributed in Yazd, Iran using PCR–RFLP. Journal of Food Quality and Hazards Control, 1, 15–20. http://jfqhc.ssu.ac.ir/article-1-47-en.html
Hamidinejat H., Razi Jalali M. H., Gharibi D., & Molayan P. H. (2015). Detection of Sarcocystis spp. in cattle (Bos taurus) and water buffaloes (Bubalus bubalis) in Iran by PCR-RFLP. Journal of Parasitic Diseases, 39, 658–662. https://doi.org/10.1007/s12639-014-0426-6
Hamidinejat H., Jalali M. H., & Nabavi L. (2010). Survey on Sarcocystis infection in slaughtered cattle in South-West of Iran, emphasized on evaluation of muscle squash in comparison with digestion method. Journal of Animal and Veterinary Advances, 9, 1724-1726. https://doi.org/10.3923/javaa.2010.1724.1726
Hoeve-Bakker B. J., van der Giessen J. W., & Franssen F. J. (2019). Molecular identification targeting cox1 and 18S genes confirms the high prevalence of Sarcocystis spp. in cattle in the Netherlands. International Journal for Parasitology, 49, 859–66. https://doi.org/10.1016/j.ijpara.2019.05.008
Hooshyar H., Abbaszadeh Z., Sharafati-Chaleshtori R., & Arbabi M. (2017). Molecular identification of Sarcocystis species in raw hamburgers using PCR-RFLP method in Kashan, central Iran. Journal of Parasitic Diseases, 41, 1001–1005. https://doi.org/10.1007/s12639-017-0925-3
Hornok S., Mester A., Takacs N., Baska F., Majoros G., Fok E., Biksi I., Nemet Z., Hornyak A., Janosi S., & Farkas R. (2015). Sarcocystis infection of cattle in Hungary. Parasites & Vectors, 8, 69-75. https://doi.org/10.1002/9781118649985.ch9
Hussein S. N., Ibrahim A. A., & Shukur M. S. (2023). Histopathology and molecular identification of Sarcocystis species forming macrocysts in slaughtered sheep and goats of Duhok, Iraq. Veterinary Research Forum, 14, 415-422. https://doi.org/10.30466/vrf.2023.559514.3575
Ibrahim M., El Sabagh H., Wahba R.A., & Abd El Rahman, E. S. (2018). The Incidence of Sarcocystis in Slaughtered Food Animals. Benha Veterinary Medicine Journal, 35, 106-122. https://doi.org/10.21608/bvmj.2018.38219
Imre K., Darabus G., Tirziu E., Morariu S., Imre M., Plutzer J., Boldea M. V and Morar A. (2019). Sarcocystis spp. in Romanian slaughtered cattle: Molecular characterization and epidemiological significance of the findings. Biomed Research International, 4123154. https://doi.org/10.1155/2019/4123154
Italiano C. M., Wong K. T., AbuBakar S., Lau Y. L., Ramli N., Syed O. S., Kahar Bador M., & Tan C.T. (2014). Sarcocystis nesbitti causes acute, relapsing febrile myositis with a high attack rate: Description of a large outbreak of muscular sarcocystosis in Pangkor Island, Malaysia, 2012. PLoS Neglected Tropical Diseases, 8, e2876. https://doi.org/10.1371/journal.pntd.0002876
Jehle C., Dinkel A., Sander A., Morent M., Romig T., Luc P. V., De T. V., Thai V. V., & Mackenstedt U. (2009). Diagnosis of Sarcocystis spp. In cattle (Bos Taurus) and water buffalo (Bubalus bubalis) in northern Vietnam. Veterinary Parasitology, 166, 314–320. https://doi.org/10.1016/j.vetpar.2009.08.024
JyothiSree C., Venu R., Samatha V., Malakondaiah P., & Rayulu V. C. (2017). Prevalence and microscopic studies of Sarcocystis infection in naturally infected water buffaloes (Bubalus bubalis) of Andhra Pradesh. Journal of Parasitic Diseases, 41, 476-482. https://doi.org/10.1007/s12639-016-0832-z
Khairy N., Ayman M. A., Mounir M. B., Ahmed F., Bahaa S. M., Nermeen M. L., Ghada H., Maher Z. M., Salem M. M., & Abdelhaseib M. (2024). Advancing meat safety diverse approaches for bovine tuberculosis detection and control in abattoirs. Italian Journal of Food Science, 36, 240-254. https://doi.org/10.15586/ijfs.v36i4.2660
Khalifa R. M., El-Nadi N. A., Sayed F. G., & Omran E. K. (2008). Comparative morphological studies on three Sarcocystis species in Sohag, Egypt. J. Egypt. Soc. Parasitol. 38: 599-608.
Lawan F. A., Ejeh E. F., Waziri A., Kwanashie C. N., Kadima K. B., & Kazeem H. M. (2020). Prevalence of Tuberculosis in Cattle Slaughtered at Maiduguri Central ‎Abattoir, Nigeria. Sahel Journal of Veterinary Sciences, 17, 14-21. https://doi.org/10.54058/saheljvs.v17i3.167
Lindsay D. S., & Dubey J. P. (2020). Neosporosis, toxoplasmosis, and sarcocystosis in ruminants: An update. Veterinary Clinics of North America: Food Animal Practice, 36, 205-222. https://doi.org/10.1016/j.cvfa.2019.11.004
Ministry of Egyptian Agriculture: Law 53 for 1966 and 207 for 1980. https://api.worldanimalprotection.org/country/egypt
Moré G., Basso W., Bacigalupe D., Venturini M. C., & Venturini L. (2008). Diagnosis of Sarcocystis cruzi, Neospora caninum and Toxoplasma gondii infections in cattle. Parasitology Research, 102, 671-675. https://doi.org/10.1007/s00436- 007-0810-6
Mounika K., Chennuru S., Ravipati V., Tumati S. R., & Krovvidi S. (2018). Studies on prevalence and histomorphology of Sarcocystis species infecting cattle in Andhra Pradesh, India. Journal of Parasitic Diseases, 42, 77-80. https://doi.org/10.1007/s12639-017-0968-5
Mousa M. M., El Sokkary M. Y., Hamouda A., Walaa S., & Hegazy M. A. (2021). The Prevalence of Sarcocystis Affecting Slaughtered Cattle and Buffalo at SirsElian Abattoir in Egypt. Alexandria Journal of Veterinary Science, 69, 49-58. https://www.bibliomed.org/gotodoi.php?mno=125880&gdoi=10.5455/ajvs.125880
Nahed H., Ghoneim W. M., & Nader M. S. (2014). Occurrence of zoonotics sarcosporidiosis in slaughtered cattle and buffaloes in different abattoirs in Egypt. Global Veterinaria, 13(5), 809-813. https://doi.org/10.5829/idosi.gv.2014.13.05.86211
Nance J. P., Vannella K. M., Worth D., David C., Carter D., Noor S., Hubeau C., Fitz L., Lane T. E., & Wynn T. A. (2012). Chitinase dependent control of protozoan cyst burden in the brain. PLoS Pathogens, 8, e1002990. https://doi.org/10.1371/journal.ppat.1002990
Obijiaku, I. N., Ajogi, I., Umoh, J. U., Lawal, I. A., & Atu, B. O. (2013). Sarcocystis infection in slaughtered cattle in Zango abattoir, Zaria, Nigeria. Veterinary World, 66, 346-349. https://doi.org/10.5455/vetworld.2013.346-349
Oğuz B., Değer M. S., & Koşal S. (2021). Molecular identification using 18S ribosomal RNA of Sarcocystis spp. In bovine minced meat in Van Province, Turkey. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 68, 97–105. https://doi.org/10.33988/auvfd.671606
Ota T., Nakano Y., Mizuno T., Shiozaki A., Hori Y., Yamanishi K., Hayakawa K., Hayakawa T., Fujimoto T., Nakamoto C., Maejima K., Wada Y., Terasoma F., & Ohnishi T. (2019). First case report of possible Sarcocystis truncata-induced food poisoning in venison. Internal Medicine, 58, 2727-2730. https://doi.org/10.2169/internalmedicine
Portella L. P., Fernandes F. Rodrigues F. S., Minuzzi C. E., Sangioni L.A., Flores M. M., & Vogel F. S. (2021). Macroscopic, histological, and molecular aspects of Sarcocystis spp. infection in tissues of cattle and sheep. Revista Brasileira de Parasitologia Veterinária, 30, e003621. https://doi.org/10.1590/S1984-29612021050
Prakas P., Strazdaitė-Žielienė Ž., Januškevičius V., Chiesa F., Baranauskaitė A., Rudaitytė-Lukošienė E., Servienė E., Petkevičius S., & Butkauskas D. (2020). Molecular identification of four Sarcocystis species in cattle from Lithuania, including S. hominis, and development of a rapid molecular detection method. Parasites & Vectors, 13, 1-9. https://doi.org/10.1186/s13071-020-04473-9.
Sarafraz N., Spotin A., Haniloo A., & Fazaeli, A. (2020). Prevalence and molecular analysis of Sarcocystis infections in cattle in Northwest Iran and the first global report of S. gigantea in cattle. Microbiology and Infectious Diseases, 73, 101566. https://doi.org/10.1016/j.cimid.2020.101566
Shahraki M. K., Ghanbarzehi A., & Dabirzadeh M. (2018). Prevalence and histopathology of Sarcocystosis in slaughtered carcasses in southeast Iran. Journal of Advanced Veterinary and Animal Research, 5, 381-387. https://doi.org/10.5455/javar.2018.e288
Shekarforoush S., Razavi S., & Abbasvali M. (2013). First detection of Sarcocystis hirsuta from cattle in Iran. Iranian Journal of Veterinary Research, 14, 155-157. https://doi.org/10.22099/ijvr. 2013.1591
Shosha E. A., Zanaty A. M., Darwesh M. M., & Fotouh A. (2024). Molecular characterization and immunopathological investigation of Avian reticuloendotheliosis virus in breeder flocks in Egypt. Virology Journal, 21, 259. https://doi.org/10.1186/s12985-024-02525-5
Thrusfield M., Christley R., & Brown H. (2017). Veterinary Epidemiology (4th ed.). Wiley-Blackwell. Edinburgh, UK.
Yang Y., Dong H., Su, R., Wang Y., Wang R., Jiang Y., & Tong Z. (2018). High prevalence of Sarcocystis spp. infections in cattle Bostaurus from central China. Parasite International, 67(6), 800-804. https://doi.org/10.1016/j.parint.2018.08.006
Zeng H., Van Damme I., Kabi T. W., Barbara S., & Sarah G. (2021). Sarcocystis species in bovine carcasses from a Belgian abattoir: a cross-sectional study. Parasites & Vectors, 14, 271. https://doi.org/10.1186/s13071-021-04788-1