PREVALENCE OF Staphylococcus aureus AND Salmonella SPECIES IN CHICKEN MEAT PRODUCTS RETAILED IN EGYPT
DOI:
https://doi.org/10.26873/SVR-1666-2022Keywords:
chicken meat products, Staphylococcus aureus, Salmonella species, EgyptAbstract
Chicken meat products represent an important source of animal derived proteins, vitamins, and minerals. However, chicken meat products might act as potential sources of human exposure to foodborne pathogens such as Staphylococcus aureus (S. aureus) and Salmonella species. The objectives of the present study were first to investigate the prevalence rates of S. aureus and Salmonella species in the retailed chicken meat products at Zagazig city, Egypt. Second, serological identification of the isolated bacteria was followed. Third, screening of S. aureus enterotoxin coding genes (sea seb, and sed) as well as Salmonella virulence associated genes including invA, Salmonella hyper-invasive locus (hilA), and Salmonella enterotoxin (stn) was done using PCR. The obtained results revealed isolation of S. aureus from the examined chicken meat products at 22%, and Salmonella spp., at 6.66%. Where S. aureus was isolated at 33.33%, 36.66%, 13.33%, 6.66%, and 20% from the examined chicken burger, fillet, luncheon, nuggets, and panne, respectively. Salmonella spp. could be isolated only from chicken burger and fillet at 10%, and 23.33%, respectively. The recovered S. aureus isolates harbored enterotoxin coding genes (sea, and seb). Likely the recovered Salmonella spp. isolates harbored virulence associated genes such as invA, hilA, and stn. Moreover, antimicrobial sensitivity testing of the recovered isolates showed multidrug resistance profiling. In conclusion, chicken meat products retailed in Egypt might be potential sources for the spread of multidrug resistant S. aureus and Salmonella spp. Therefore, strict hygienic measures should be adopted during manufacturing of such meat products.
References
● 1. El Bayomi RM, Darwish WS, Elshahat SS, Hafez AE. 2018. Human health risk assessment of heavy metals and trace elements residues in poultry meat retailed in Shark-ia Governorate, Egypt. Slov Vet Res. 2018; 55(Suppl 20): 211–9.
● 2. Morshdy AEMA, Darwish WS, Salah El-Dien WM, Khalifa SM. 2019. Prevalence of multidrug-resistant Staphylococcus aureus and Salmonella enteritidis in meat prod-ucts retailed in Zagazig City, Egypt. Slov Vet Res 2019; 55: 295–301.
● 3. Darwish WS, Atia AS, Reda LM, et al. Chicken gib-lets and wastewater samples as possible sources of methicil-lin-resistant Staphylococcus aureus: Prevalence, enterotoxin production, and antibiotic susceptibility. J Food Safety 2018; e12478.
● 4. Morshdy AEMA, Nahla BM, Shafik S, et al. Anti-microbial effect of essential oils on multidrug-resistant Salmonella typhimurium in chicken fillets. Pak Vet J 2021; http: //dx.doi.org/10.29261/pakvetj/2021.055.
● 5. Hennekinne JA, De Buyser ML, Dragacci S. Staphy-lococcus aureus and its food poisoning toxins: Characteriza-tion and outbreak investigation. FEMS Microbiol Rev 2012; 36: 815–36.
● 6. Abolghait SK, Fathi AG, Youssef FM, et al. Methi-cillin-resistant Staphylococcus aureus (MRSA) isolated from chicken meat and giblets often produces staphylococcal enterotoxin B (SEB) in non-refrigerated raw chicken livers. Int J Food Microbiol. 2020; 328: 108669.
● 7. Neyaz L, Rajagopal N, Wells H, et al. Molecular characterization of Staphylococcus aureus plasmids associated with strains isolated from various retail meats. Front Micro-biol 2020; 11: 223.
● 8. Rortana C, Nguyen-Viet H, Tum S, et al. Prevalence of Salmonella spp. and Staphylococcus aureus in chicken meat and pork from Cambodian markets. Pathogens 2021; 10(5): 556.
● 9. Sams AR. Poultry meat processing Chap. 9, ISBN – 0120-3, CRC Press LLC. New York, USA. 2001.
● 10. Luu QH, Fries R, Padungtod P, et al. Prevalence of Salmonella in retail chicken meat in Hanoi, Vietnam. Ann N Y Acad Sci 2006; 1081: 257–61.
● 11. Iwabuchi E, Yamamoto S, Endo Y, et al. Preva-lence of Salmonella isolates and antimicrobial resistance patterns in chicken meat throughout Japan. J Food Prot 2011; 74(2): 270-–3.
● 12. Darwish WS, Eldaly EA, El-Abbasy MT, Ikenaka Y, Nakayama S, Ishizuka M. Antibiotic residues in food: the African scenario. Jpn J Vet Res 2013; 61(Supplement): S13–22.
● 13. Alsayeqh AF, Baz AH, Darwish WS. Antimicro-bial-resistant foodborne pathogens in the Middle East: A systematic review. Environ Sci Pollut Res 2021; 19: 1–23.
● 14. American Public Health Association (APHA) Compendium of methods for the microbiological examina-tion of food, 4th Ed., Washington. 2001.
● 15. ISO (International Standard Organization) 6579: 4th ed. Microbiology - General guidance on methods for the detection of Salmonella, International Organization for Standardization, Geneve, Switzerland. 2002(E).
● 16. Mehrotra M, Wang G, Johnson WM. Multiplex PCR for Detection of Genes for Staphylococcus aureus entero-toxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000; 38 (3): 1032–5.
● 17. Murugkar HV, Rahman H, Dutta PK. Distribu-tion of virulence genes in Salmonella serovars isolated from man & animals. Indian J Med Res 2003; 117: 66–70.
● 18. Cardona-Castro N, Restrepo-Pineda E, Correa-Ochoa M. Detection of hilA Gene Sequences in Serovars of Salmonella enterica Subspecies Enterica. Mem Inst Oswaldo Cruz 2002; 97(8): 1153–6.
● 19. Morshdy AE, Hussein MA, Tharwat AE, et al. Prevalence of enterotoxigenic and multi-drug-resistant Staphylococcus aureus in ready to eat meat sandwiches. Slov Vet Res 2018c; 55: 367–74.
● 20. Hanson BM, Dressler AE, Harper AL, et al. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health 2011; 4(4): 169–74.
● 21. Feßler AT, Kadlec K, Hassel M, et al. Characteri-zation of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl Environ Microbiol 2011; 77(20): 7151–7.
● 22. Akbar A, Anal AK. Prevalence and antibiogram study of Salmonella and Staphylococcus aureus in poultry meat. Asian Pac J Trop Biomed 2013; 3(2): 163–8.
● 23. Momtaz H, Dehkordi FS, Rahimi E, et al. Viru-lence genes and antimicrobial resistance profiles of Staphy-lococcus aureus isolated from chicken meat in Isfahan prov-ince, Iran. J Appl Poul Res 2013; 22(4): 913–21.
● 24. Centers for Disease Control and Prevention (CDC). Outbreak of Staphylococcal Food Poisoning from a Military Unit Lunch Party - United States, July 2013. 62(50): 1026–8.
● 25. European Food Safety Authority (EFSA). Euro-pean Centre for Disease Prevention and Control. The Eu-ropean Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Foodborne Outbreaks in 2009. EFSA J 2011; 9(3): 2090.
● 26. Argudín MÁ, Mendoza MC, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins. Toxins 2010; 2(7): 1751–73.
● 27. Darwish WS, El-Ghareeb WR, Alsayeqh AF, Morshdy AE. Foodborne intoxications and toxicoinfec-tions in the Middle East. InFood Safety in the Middle East 2022 Jan 1 (pp. 109–41). Academic Press.
● 28. Pepe O, Blaiotta G, Bucci F, et al. Staphylococcus au-reus and staphylococcal enterotoxin A in breaded chicken products: detection and behavior during the cooking pro-cess. Appl Environ Microbiol 2006; 72(11): 7057–62.
● 29. Sarrafzadeh Zargar MH, Hosseini Doust R, Mohebati Mobarez A. Staphylococcus aureus enterotoxin A gene isolated from raw red meat and poultry in Tehran, Iran. Int J Enteric Pathog 2014; 2(3): 1–6.
● 30. Amoako DG, Somboro AM, Abia AL, et al. An-tibiotic resistance in Staphylococcus aureus from poultry and poultry products in uMgungundlovu District, South Africa, using the “Farm to Fork” approach. Microb Drug Resis 2020; 26(4): 402–11.
● 31. Zakaria Z, Hassan L, Sharif Z, et al. Analysis of Salmonella enterica serovar Enteritidis isolates from chickens and chicken meat products in Malaysia using PFGE, and MLST. BMC Vet Res 2020; 16(1): 393.
● 32. Chittick P, Sulka A, Tauxe RV, Fry AM. A sum-mary of national reports of foodborne outbreaks of Salmo-nella Heidelberg infections in the United States: clues for disease prevention. J Food Prot 2006; 69(5): 1150–3.
● 33. Schmid H, Hachler H, Stephan R, et al. Outbreak of Salmonella enterica serovar Typhimurium in Switzerland, May-June 2008, implications for production and control of meat preparations. Euro Surveill 2008; 13(44): pii: 19020.
● 34. Cleary P, Browning L, Coia J, et al. A foodborne outbreak of Salmonella Bareilly in the United Kingdom, 2010. Euro Surveill 2010; 15(48): 19732.
● 35. Ford L, Wang Q, Stafford R, et al. Seven Salmonel-la Typhimurium outbreaks in Australia linked by trace-back and whole genome sequencing. Foodborne Pathog Dis 2018; 15(5): 285–92.
● 36. Prager R, Fruth A, Tschape H. Salmonella entero-toxin (stn) gene is prevalent among strains of Salmonellaen-terica, but not among Salmonellabongori and other Enter-obacteriaceae. FEMS Immunol Med Microbiol 1995; 12(1): 47–50.
● 37. Boddicker JD, Knosp BM, Jones BD. Transcrip-tion of the Salmonella invasion gene activator, hilA requires HilD activation in the absence of negative regulators. J Bacteriol 2003; 185(2): 525–33.
● 38. Parvin MS, Hasan MM, Ali MY, et al. Prevalence and multidrug resistance pattern of Salmonella carrying ex-tended-spectrum β-Lactamase in frozen chicken meat in Bangladesh. J Food Prot 2020; 83(12): 2107–21.
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Copyright (c) 2023 Alaa Eldin M. A. Morshdy, Abdallah Fikry A. Mahmoud, Sahar M. Khalifa, Waiel M. Salah El-Dien, Wageh Sobhy Darwish, Rasha El Bayomi
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