PREVALENCE OF STAPHYLOCOCCUS AUREUS AND SALMONELLA SPECIES IN RETAILED CHICKEN MEAT WITH A REDUCTION TRIAL USING NIGELLA SATIVA AND ROSEMARY ESSENTIAL OILS
DOI:
https://doi.org/10.26873/SVR-1449-2021Keywords:
hicken muscles, Staphylococcus aureus, Salmonella species, Nigella sativa, rosemary essen-tial oilsAbstract
Chicken meat represents an importance source of animal derived proteins, vitamins, and minerals. However, chicken meat might act as a potential source 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 breast and thigh muscles at Zagazig city, Egypt. Second, serological identification of the isolated bacteria was followed. Third, screening of S. aureus enterotoxin coding genes (sea, seb, sec, sed, and see) and methicillin resistance (mecA) gene, as well as Salmonella virulence associated genes including Salmonella hyper-invasive locus (hilA), and Salmonella enterotoxin (stn) was done using PCR. Thereafter, the inhibitory effects of Nigella sativa, and rosemary essential oils were investigated against S. aureus, and Salmonella Typhimurium. The obtained results revealed isolation of S. aureus from the examined breast and thigh muscles at percentages of 23.3%, and 26.6%, respectively, whereas percentages of Salmonella spp. isolation from both samples were 33.3%, and 16.6%, respectively. Four Salmonella serotypes namely, S. Typhimurium, S. Enteritidis, S. Kentucky, and S. Anatum were further identified. The recovery rates of S. Typhimurium from breast and thigh muscles were 23.33% and 13.33%, respectively followed by S. Enteritidis (3.33% each). Staphylococcus enterotoxin genes (sea, and see), and mecA gene were detected in S. aureus isolates. Besides, Salmonella hilA and stn genes were also detected in Salmonella Typhimurium isolates. Nigella sativa and rosemary essential oils at 0.1%, and 0.5% could significantly reduce S. aureus, and Salmonella Typhimurium in chicken breast meat.
References
● 1. Darwish WS, Atia AS, Reda LM, et al. Chicken giblets and wastewater samples as possible sources of methicillin-resistant Staphylococcus aureus: Prevalence, enterotoxin production, and antibiotic susceptibility. J Food Safety 2018; 38: e12478.
● 2. Morshdy AEMA, Nahla BM, Shafik S, et al. Antimicrobial 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.
● 3. Abd-Elghany SM, Sallam KI, Abd-Elkhalek A, et al. Occurrence, genetic characterization and antimi-crobial resistance of Salmonella isolated from chicken meat and giblets. Epidemiol Infect 2015; 143: 997–1003.
● 4. Darwish WS, Saad Eldin WF, Eldesoky KI. Prevalence, molecular characterization and antibiotic susceptibility of Escherichia coli isolated from duck meat and giblets. J Food Safety 2015; 35: 410–5.
● 5. Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation. FEMS Microbiol Rev 2012; 36: 815–36.
● 6. Abolghait SK, Fathi AG, Youssef FM, et al. Methicillin-resistant Staphylococcus aureus (MRSA) iso-lated 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 asso-ciated with strains isolated from various retail meats. Front Microbiol 2020; 11: 223.
● 8. Rortana C, Nguyen-Viet H, Tum S, et al. Preva-lence of Salmonella spp. and Staphylococcus aureus in chicken meat and pork from Cambodian markets. Pathogens 2021; 10: 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. Preva-lence 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. Prevalence of Salmonella isolates and antimicrobial resistance patterns in chicken meat throughout Japan. J Food Prot 2011; 74: 270–3.
● 12. Mouwakeh A, Telbisz Á, Spengler G, et al. Antibacterial and resistance modifying activities of Nigella sativa essential oil and its active compounds against Listeria monocytogenes. In Vivo 2018; 32: 737–43.
● 13. Chraibi M, Farah A, Elamin O, et al. Character-ization, antioxidant, antimycobacterial, antimicrobial effects of Moroccan rosemary essential oil, and its synergistic antimicrobial potential with carvacrol. J Adv Pharm Technol Res 2020; 11: 25–29.
● 14. American Public Health Association (APHA) Compendium of methods for the microbiological examination 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 Organi-zation for Standardization, Geneve, Switzerland. 2002(E).
● 16. McClure JA, Conly JM, Lau V, et al. Novel multiplex PCR assay for detection of the staphylo-coccal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from-resistant staphylococci. J Clin Mi-crobiol 2006; 44: 1141–114.
● 17. Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection ofgGenes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000; 38: 1032–5.
● 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: 1153–6.
● 19. Murugkar HV, Rahman H, Dutta PK. Distribu-tion of virulence genes in Salmonella serovars isolat-ed from man & animals. Indian J Med Res 2003; 117: 66–70.
● 20. Tang H, Darwish WS, El-Ghareeb WR, et al. Microbial quality and formation of biogenic amines in the meat and edible offal of Camelus dromedaries with a protection trial using gingerol and nisin. Food Sci Nutr 2020; 8: 2094–101.
● 21. Govaris A, Solomakos N, Pexara A, et al. The antimicrobial effect of oregano essential oil, nisin and their combination against Salmonella Enteritidis in minced sheep meat during refrigerated storage. Int J Food Microbiol 2010; 137: 175–80.
● 22. Maturin L, Peeler JT. 2001. Chapter 3. Aerobic Plate Count,” In: Food and Drug Administration (FDA), Bacterio-logical Analytical Manual Online, 8th Edition, Silver Spring, Berlin, 1998.
● 23. Ammar AM, Attia AM, Abd El-Aziz, et al. Class 1 integron and associated gene cassettes medi-ating multiple-drugresistance in some food borne pathogens. Int Food Res J; 23: 332–9
● 24. Abd El-Aziz NK, Abd El-Hamid MI, Bendary MM, et al. Existence of vancomycin resistance among methicillin resistant S. aureus recovered from animal and human sources in Egypt. Slov Vet Res 2018; 55: 221–30.
● 25. Abd El-Aziz NK, Tartor YH, Gharib AA, et al. Propidium monoazide quantitative real-time polymer-ase chain reaction for enumerationof some viable but nonculturable foodborne bacteria in meat and meat products. Foodborne Pathog Dis; 15: 226–34
● 26. Ge B, Mukherjee S, Hsu CH, et al. MRSA and multidrug-resistant Staphylococcus aureus in U.S. retail meats, 2010-2011. Food Microbiol 2017; 62: 289–97.
● 27. Crago B, Ferrato C, Drews SJ, et al. Prevalence of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in food samples associated with food-borne illness in Alberta, Canada from 2007 to 2010. Food Microbiol 2012; 32: 202–5.
● 28. Shawish RR, Al-Humam NA. 2016. Contamina-tion of beef products with staphylococcal classical enterotoxins in Egypt and Saudi Arabia. GMS Hyg Infect Control 2016; 11: Doc08.
● 29. Centers for Disease Control and Prevention (CDC). Outbreak of staphylococcal food poisoning from a Military Unit Lunch Party - United States, July, 2012. 2013; 62: 1026–8.
● 30. European Food Safety Authority (EFSA). Eu-ropean Centre for Disease Prevention and Control. The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2009. EFSA J 2011; 9(3): 2090.
● 31. Ammar AM, Abd El-Aziz NK, Hanafy MS, et al. Serotypes profile of avian Salmonellae and estima-tion of antibiotic residues in chicken muscles using highperformance liquid chromatography. Advances in Environmental Biology (2016); 10: 173–9
● 32. Zakaria Z, Hassan L, Sharif Z, et al. Analysis of Salmonella enterica serovar Enteritidis isolates from chickens and chicken meat products in Malaysia us-ing PFGE, and MLST. BMC Vet Res 2020; 16: 393.
● 33. Parvin MS, Hasan MM, Ali MY, et al. Prevalence and multidrug resistance pattern of Salmonella carrying extended-spectrum β-Lactamase in frozen chicken meat in Bangladesh. J Food Prot 2020; 83: 2107–21.
● 34. Schmid H, Hachler H, Stephan R, et al. Out-break of Salmonella enterica serovar Typhimurium in Switzerland, May-June 2008, implications for produc-tion and control of meat preparations. Euro Surveill 2008; 13: pii: 19020.
● 35. Ford L, Wang Q, Stafford R, et al. Seven Sal-monella Typhimurium outbreaks in Australia linked by trace-back and whole genome sequencing. Food-borne Pathog Dis 2018; 15: 285–92.
● 36. Prager R, Fruth A, Tschape H. Salmonella en-terotoxin (stn) gene is prevalent among strains of Salmonella enterica, but not among Salmonella bongori and other Enterobacteriaceae. FEMS Immunol MedMi-crobiol 1995; 12: 47–50.
● 37. Boddicker JD, Knosp BM, Jones BD. Tran-scription of the Salmonella invasion gene activator, hilA requires HilD activation in the absence of nega-tive regulators. J Bacteriol 2003; 185: 525–33.
● 38. Tartor YH, Hassan FAM. Assessment of car-vacrol for control of avian aspergillosis in intratrache-ally challenged chickens in comparison to voricona-zole with a reference on economic impact. J Appl Microbiol. 2017;123(5):1088-1099. doi: 10.1111/jam. 13557.
● 39. Gharieb, R.M.A.; Saad, M.F.; Mohamed, A.S.; Tartor, Y.H. Characterization of two novel lytic bacteriophages for reducing biofilms of zoonotic multidrug-resistant Staphylococcus aureus and controlling their growth in milk. LWT 2020, 124, doi:10.1016/j.lwt.2020.109145.
● 40. Mahboub HH, Tartor YH. Carvacrol essential oil stimulates growth performance, immune response, and tolerance of Nile tilapia to Cryptococcus unigut-tulatus infection. Dis Aquat Organ. 2020;141:1–14. doi: 10.3354/dao03506. PMID: 32940246.
● 41. Abd El-Aziz NK, Ammar AM, El-Naenaeey EYM, et al. Antimicrobial and antibiofilm potentials of cinnamon oil and silver nanoparticles against Streptococcus agalactiae isolated from bovine masti-tis: New avenues for countering resistance. BMC Vet Res 2021; 17, 1–14.
● 42. Han JH, Patel D, Kim JE, et al. Retardation of Listeria monocytogenes growth in mozzarella cheese us-ing antimicrobial sachets containing rosemary oil and thyme oil. J Food Sci 2014; 79: E2272–8.
● 43. Ugur AR, Dagi HT, Ozturk B, et al. Assess-ment of in vitro antibacterial activity and cytotoxicity effect of Nigella sativa Oil. Pharmacogn Mag 2016; 12: S471–4.
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Copyright (c) 2021 Amina H.A. Habashy, Waiel M. Salah El-Dien, Mohamed A. M. Hussein, Wageh Sobhy Darwish
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