Preview

Theory and practice of meat processing

Advanced search

Prevalence and serotyping of Salmonella in beef carcasses sold in markets of Hama city, Syria

https://doi.org/10.21323/2414-438X-2025-10-1-4-10

Abstract

Salmonella is one the most important pathogenic bacteria, which causes food poisoning in human consumers worldwide. This study aimed to detect the prevalence and serovars of Salmonella in beef in markets of Hama city, Syria. The study was carried out on 200 beef samples from 20 retail shops in markets of Hama city, Syria. Investigation was conducted using bacterial cultures and serotyping. Bacterial cultures showed that 11 samples out of 200 samples from different retail shops were positive, with an overall prevalence of 5.5% (95% CI: 2.34–8.66). The isolated serotypes were S. Typhimurium (36.36%), S. Enteritidis (27.27%), S. Reading (9.09%), S. Bredeney (9.09%), S. Chester (9.09%), and S. Anatum (9.09%). Significantly higher (p<0.05) prevalence was revealed in the east district (8%, 4/50) compared to other districts, in informal shops (7.5%, 6/80) than in other outlets, in female animals (10%, 4/40) compared to male animals, in slaughtered animals at the age of more than 12 months (7.5%; 6/80), in summer (12%, 6/50) compared to other seasons, in unclean shops (7.38%, 9/122), and in liver (7.5%, 6/80) compared to other meat types. These results are considered an important threat to public health and indicate food contamination.

About the Authors

O. Faour
Hama University
Syrian Arab Republic

Omran Faour - PhD in Epidemiology, Department of Animal Diseases, Faculty of Veterinary Medicine, Hama University. Syrian Arab Republic, Hama, Assi Square, Old Town Building, Syria-Hama — S. B.

Hama, Tel.: +963–99–195–35–17



Kh. Alkoujah
Hama University
Syrian Arab Republic

Khaldoun Alkoujah - PhD in Meat Hygiene and Technology, Department of Public Health and Preventive Medicine, Faculty of Veterinary Medicine, Hama University. Syrian Arab Republic, Hama, Assi Square, Old Town Building, Syria-Hama — S. B.

Hama, Tel.: +963–94–727–98–24



References

1. Nørrung, B., Andersen, J. K., Buncic, S. (2009). Main concerns of pathogenic microorganisms in meat. Chapter in book: Safety of meat and processed meat. Springer New York, NY, 2009. http://doi.org/10.1007/978-0-387-89026-5_1

2. Ali, S., Alsayeqh, A. F. (2022). Review of major meat-borne zoonotic bacterial pathogens. Frontiers in Public Health, 10, Article 1045599. http://doi.org/10.3389/fpubh.2022.1045599

3. Strickland, A. J., Sampedro, F., Hedberg, C. W. (2023). Quantitative risk assessment of Salmonella in ground beef products and the resulting impact of risk mitigation strategies on public health. Journal of Food Protection, 86(6), Article 100093. http://doi.org/10.1016/j.jfp.2023.100093

4. Sheng, H., Suo, J., Dai, J., Wang, S., Li, M., Su, L. et al. (2023). Prevalence, antibiotic susceptibility and genomic analysis of Salmonella from retail meats in Shaanxi, China. International Journal of Food Microbiology, 403, Article 110305. http://doi.org/10.1016/j.ijfoodmicro.2023.110305

5. Marshall, K. E., Cui, Z., Gleason, B. L., Hartley, C., Wise, M. E., Bruce, B. B. et al. (2024). An approach to describe Salmonella serotypes of concern for outbreaks: Using burden and trajectory of outbreak-related illnesses associated with meat and poultry. Journal of Food Protection, 87(9), Article 100331. http://doi.org/10.1016/j.jfp.2024.100331

6. Das, A. K., Nanda, P. K., Das, A., Biswas, S. (2019). Hazards and safety issues of meat and meat products. Chapter in a book: Food safety and human health. Academic Press, 2019. http://doi.org/10.1016/B978-0-12-816333-7.00006-0

7. Ukut, O. E., Okonko, I. O., Ikpoh, I. S., Nkang, A. O., Udeze, A. O., Babalola, T. A. et al. (2010). Assessment of bacterio-logical quality of fresh meats sold in Calabar Metropolis, Nigeria. Electronic Journal of Environmental, Agricultural and Food Chemistry, 9(1), 89–100.

8. Adzitey, F., Teye, G. A., Kutah, W. N., Adday, S. (2011). Microbial quality of beef sold on selected market in the Tamale Metropolis in the northern region of Ghana. Livestock Research for Rural Development, 23(1), 54–63.

9. Sayed, H. K., Tolba, K. S., Sobhy, H. M., Hekal, S. H. A. (2021). Assuring the safety of local and imported beef meat from different slaughterhouses in Egypt. Advanced Animal Veterinary Sciences, 9(9), 1472–1482. http://doi.org/10.17582/journal.aavs/2021/9.9.1472.1482

10. Biswas, A. K., Kondaiah, A. K., Anjaneyulu, A. S., Mandal, P. K. (2011). Causes, concerns, consequences and control of microbial contaminants in meat. International Journal of Meat Science, 1(1), 27–35. http://doi.org/10.3923/ijmeat.2011.27.35

11. Soyiri, I. N., Agbogli, H. K., Dongdem, J. T. (2008). A pilot microbial assessment of beef sold in the Ashaiman market, a suburb of Accra. African Journal of Food, Agriculture, Nutrition and Development, 8(1), 91–103. http://doi.org/10.4314/ajfand.v8i1.19182

12. World Health Organization. (2015). WHO estimates of the global burden of foodborne diseases: Foodborne diseases burden epidemiology reference group 2007–2015 Retrieved from https://www.who.int/publications/i/item/9789241565165 Accessed September 9, 2024.

13. Jajere, S. M. (2019). A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Veterinary World, 12(4), 504–521. http://doi.org/10.14202/vetworld.2019.504-521

14. Centers for Disease Control and Prevention. (2024). Salmonella (Non-Typhoidal). Retrieved from https://wwwnc.cdc.gov/travel/yellowbook/2024/infections-diseases/salmonellosis-nontyphoidal#:~:text=Nontyphoidal%20Salmonella%20infection%20usually%20presents,treatment%20after%201%E2%80%937%20days Accessed September 9, 2024.

15. Ribot, E. M., Fair, A. M., Gautom, R., Cameron, D.N., Hunter, S.B., Swaminathan, B. et al. (2006). Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157: H7, Salmonella, and Shigella for PulseNet. Foodborne Pathogens and Disease, 3(1), 59–67. http://doi.org/10.1089/fpd.2006.3.59

16. Xu D., Chen L., Lu Z., Wu X. (2024). Prevalence and serotyping of Salmonella in retail food in Huzhou China. Journal of Food Protection, 87(2), Article 100219. http://doi.org/10.1016/j.jfp.2024.100219

17. Carter, G. R., Cole Jr, J. R. (2012). Diagnostic procedure in veterinary bacteriology and mycology. Academic Press, 2012.

18. Ryan, M. P., O’Dwyer, J., Adley, C. C. (2017). Evaluation of the complex nomenclature of the clinically and veterinary significant pathogen Salmonella. BioMed Research International, 2017, Article 3782182 http://doi.org/10.1155/2017/3782182

19. Mahon, C. R., Lehman, D. C. (2022). Textbook of Diagnostic Microbiology-E-Book. Elsevier Health Sciences, 2022.

20. Centers for Disease Control and Prevention. (2021). Salmonella. Retrieved from https://www.cdc.gov/salmonella/about/index.html Accessed September 15, 2024.

21. Canning, M., Birhane, M. G., Dewey-Mattia, D., Lawinger, H., Cote, A., Gieraltowski, L. et al. (2023). Salmonella outbreaks linked to beef, United States, 2012–2019. Journal of Food Protection, 86(5), Article 100071. http://doi.org/10.1016/j.jfp.2023.100071

22. Iulietto, M. F., Evers, E. G. (2024). Cross‐contamination in the kitchen: A model for quantitative microbiological risk assessment. Risk Analysis, 44(5), 1156–1175. http://doi.org/10.1111/risa.14232

23. Hassanein, R., Hassan Ali, S.F., Abd El-MAlek, A.M., Moemen, Mohamed, A., Elsayh, K.B. (2011). Detection and identification of Salmonella species in minced beef and chicken meats by using multiplex PCR in Assiut City. Veterinary World, 4(1), 5–11. http://doi.org/10.5455/vetworld.2011.5-11

24. Castro-Vargas, R. E., Herrera-Sánchez, M. P., Rodríguez-Hernández, R., Rondón-Barragán, I. S. (2020). Antibiotic resistance in Salmonella spp. isolated from poultry: A global overview. Veterinary World, 13(10), 2070–2084. http://doi.org/10.14202/vetworld.2020.2070-2084

25. Malorny, B., Junker, E., Helmuth, R. (2008). Multi-locus variable-number tandem repeat analysis for outbreak studies of Salmonella enterica serotype Enteritidis. BMC Microbiology, 8, Article 84. http://doi.org/10.1186/1471-2180-8-84

26. OECD/FAO (2016). OECD-FAO Agricultural Outlook 2016–2025. OECD Publishing, Paris. http://doi.org/10.1787/agr_outlook-2016-en

27. Carron, M., Chang, Y. -M., Momanyi, K., Akoko, J., Kiiru, J., Bettridge, J. et al. (2018). Campylobacter, a zoonotic pathogen of global importance: Prevalence and risk factors in the fastevolving chicken meat system of Nairobi, Kenya. PLoS Neglected Tropical Diseases, 12(8), Article e0006658. http://doi.org/10.1371/journal.pntd.0006658

28. Jones, B. A., Grace, D., Kock, R., Alonso, S., Rushton, J., Said, M. Y. et al. (2013). Zoonosis emergence linked to agriculturalintensification and environmental change. Proceedings of the National Academy of Sciences, 110(21), 8399–8404. http://doi.org/10.1073/pnas.1208059110

29. Quinn, P. J., Marky, B. K., Leonard, F. C., FitzPatrick, E. S., Fanning, S., Hartigan, P. J. (2011). Veterinary microbiology and microbial disease. A John Wiley and Sons, Ltd., 2011.

30. Grimont, P. A. D., Weill, F. X. (2007). Antigenic formulas of Salmonella serovars WHO Collaborating Centre for Research on Salmonella, Institute Pasteur, Paris. 2007.

31. Gutema, F. D., Agga, G.E., Abdi, R. D., De Zutter, L., Duchateau, L., Gabriël, S. (2019). Corrigendum: Prevalence and serotype diversity of Salmonella in apparently healthy cattle: Systematic review and meta-analysis of published studies, 2000–2017. Frontiers in Veterinary Science, 6, Article 184. https://doi.org/10.3389/fvets.2019.00184

32. Manios, S. G., Skandamis, P. N. (2015). Effect of frozen storage, different thawing methods and cooking processes on the survival of Salmonella spp. and Escherichia coli O157: H7 in commercially shaped beef patties. Meat Science, 101, 25–32. http://doi.org/10.1016/j.meatsci.2014.10.031

33. Shilangale, R. P., Kaaya, G. P., Chimwamurombe, P. M. (2015). Prevalence and characterization of Salmonella isolated from beef in Namibia. European Journal of Nutrition and Food Safety, 5(4), 267–274. http://doi.org/10.9734/EJNFS/2015/17276

34. Bingol, E.B., Dumen, E., Kahraman, T., Akhan, M., Issa, G., Ergun, O. (2013). Prevalence of Salmonella spp., Listeria monocytogenes and Escherichia coli O157 in meat and meat products consumed in Istanbul. Medycyna Weterynaryjna, 69(8), 488–491.

35. Soltan-Dallal, M.M., Sharifi-Yazdi, M.K., Mirzaei, N., Kalantar, E. (2014). Prevalence of Salmonella spp. in packed and unpacked red meat and chicken in south of Tehran. Jundishapur Journal of Microbiology, 7(4), Article e9254. http://doi.org/0.5812/jjm.9254

36. Shafini, A. B., Son, R., Mahyudin, N. A., Rukayadi, Y., Tuan Zainazor, T. T. (2017). Prevalence of Salmonella spp. In chicken and beef from retail outlets in Malaysia. International Food Research Journal, 24(1), 437–449.

37. Van, T.T.H., Moutafis, G., Istivan, T., Tran, L.T., Coloe, P.J. (2007). Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Applied and Environmental Microbiology, 73(21), 6885–6890. http://doi.org/10.1128/AEM.00972-07

38. Phan, T.T., Khai, L.T., Ogasawara, N., Tam, N.T., Okatani, A.T., Akiba, M. et al. (2005). Contamination of Salmonella in retail meats and shrimps in the Mekong delta, Vietnam. Journal of Food Protection, 68(5), 1077–1080. http://doi.org/10.4315/0362-028X-68.5.1077

39. Oueslati, W., Rjeibi, M. R., Mhadhbi, M., Jbeli, M., Zrelli, S., Ettriqui, A. (2016). Prevalence, virulence and antibiotic susceptibility of Salmonella spp. strains, isolated from beef in Greater Tunis (Tunisia). Meat Science, 119, 154–159. http://doi.org/10.1016/j.meatsci.2016.04.037

40. Ahmed, M., Bashir, B., Abdilahi, M., Mahamed, S. (2024). Prevalence of Salmonella and Escherichia coli and associated risk factors among camel and bovine meat slaughtered at Jigjiga Municipal Abattoir, Somali Regional State, Ethiopia. Journal of Basic and Applied Research in Biomedicine, 10(1), 6–10. http://doi.org/10.51152/jbarbiomed.v10i1.233

41. Hawwas, H. A. E. H., Aboueisha, A. -K. M., Fadel, H. M., El-Mahallawy, H. S. (2022). Salmonella serovars in sheep and goats and their probable zoonotic potential to humans in Suez Canal Area, Egypt. Acta Veterinaria Scandinavica, 64(1), Article 17. http://doi.org/10.1186/s13028-022-00637-y

42. Calle, A., Carrascal, A. K., Patiño, C., Carpio, C., Echeverry, A., Brashears, M. (2021). Seasonal effect on Salmonella, Shiga toxin-producing E. coli O157: H7 and non-O157 in the beef industry in Colombia, South America. Heliyon, 7(7), Article e07547. http://doi.org/10.1016/j.heliyon.2021.e07547

43. Ekli, R., Adzitey, F., Huda, N. (October 10–11, 2018). Prevalence of resistant Salmonella spp. isolated from raw meat and liver of cattle in the Wa Municipality of Ghana. IOP Conference Series: Earth and Environmental Science, Volume 287, International Conference on Animal Production for Food Sustainability. Padang, Indonesia. http://doi.org/10.1088/1755-1315/287/1/012006

44. Brichta–Harhay, D.M., Arthur, T.M., Bosilevac, J.M., Kalchayanand, N., Shackelford, S.D., Wheeler, T.L. et al. (2011). Deversity of multidrug–resistant Salmonella enterica strains associated with cattle at harvest in the United States. Applied and Environmental Microbiology, 77(5), 1783–1796. http://doi.org/10.1128/AEM.01885-10

45. Geresu, M. A., Wayuo, B. A., Kassa, G. M. (2021). Occurrence and antimicrobial susceptibility profile of Salmonella isolates from animal origin food items in selected areas of Arsi zone, southeastern Ethiopia, 2018/19. International Journal of Microbiology, 2021, Article 6633522. http://doi.org/10.1155/2021/6633522

46. Siriken, B., Al, G., Erol, I. (2020). Prevalence and antibiotic resistance of Salmonella Enteritidis and Salmonella Typhimurium in ground beef and meatball samples in Samsun, Turkey. Microbial Drug Resistance, 26(2), 136–144. http://doi.org/10.1089/mdr.2018.0481

47. Manafi, L., Aliakbarlu, J., Saei, H. D. (2020). Antibiotic resistance and biofilm formation ability of Salmonella serotypes isolated from beef, mutton, and meat contact surfaces at retail. Journal of Food Science, 85(8), 2516–2522. http://doi.org/10.1111/1750-3841.15335

48. Koondhar, M. N., Kamboh, A. A., Khan, M. A., Leghari, R. A., Dewani, P. (2021). Antimicrobial resistance profile of Salmonella spp. isolated from raw beef meat samples collected from Karachi, Pakistan. Pakistan Journal of Zoology, 53(6), 2001–2521. http://doi.org/10.17582/journal.pjz/20190929130949


Review

For citations:


Faour O., Alkoujah Kh. Prevalence and serotyping of Salmonella in beef carcasses sold in markets of Hama city, Syria. Theory and practice of meat processing. 2025;10(1):4-10. https://doi.org/10.21323/2414-438X-2025-10-1-4-10

Views: 1012


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2414-438X (Print)
ISSN 2414-441X (Online)