INCIDENCE AND CHARACTERIZATION OF ANTIMICROBIAL RESISTANCE OF Escherichia coli IN FAST FOOD WITH SPECIAL REFERENCE TO THE ANTIBACTERIAL EFFECTS OF CINNAMON AND OREGANO ESSENTIAL OILS AGAINST E. coli O157:H7 IN MINCED MEAT

Authors

  • Alaa Eldin M. A. Morshdy Food Control Department, Faculty of Veterinary Medicine Zagazig University, Egypt
  • Mohamed A. Hussein Food Control Department, Faculty of Veterinary Medicine Zagazig University, Egypt
  • Abdallah M.A. Merwad Department of Zoonoses, Faculty of Veterinary Medicine, Zagazig University, Egypt; merwad.abdallah@yahoo.com
  • Hanan M. El. Lawendy Animal Health Research Institute, Food Hygiene Department, Zagazig, Provential Laboratory, Egypt
  • Afaf H. Mohamed Animal Health Research Institute, Food Hygiene Department, Zagazig, Provential Laboratory, Egypt
  • Taisir Saber Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia

DOI:

https://doi.org/10.26873/SVR-1458-2021

Keywords:

Escherichia coli, incidence, resistance, essential oils, fast food

Abstract

This study aimed to investigate the incidence and phenotypic and genotypic resistance of Escherichia coli isolates recovered from fast food in Sharkia Governorate, Egypt, as well as to evaluate the cinnamon and oregano essential oils treatments for inoculated minced meat with E. coli serotype O157:H7. The highest incidence of E. coli was found to be 44% in smoked herring, followed by kofta (40%), shawarma (36%), sausage (32%) and fried shrimp (24%). E. coli isolates were serotyped into O157:H7 (12.5%) and O128:H2 (12.5%) from kofta samples, O125:H21(25%) from both of sausage and fried shrimp, O119:H6 (12.5%) and O86a:H3 (12.5%) from shawarma; and O158:H7 (25%) from smoked herring. Six isolates belonging to E. coli serotypes O157, O158, O119, O128, O125 and O86a showed maximum resistance (100%) to erythromycin, gentamicin, cefepime, streptomycin, ampicillin, chloramphenicol and tetracycline. Moreover, 4 E. coli strains belonging to O157, O128, O125 and O86a serotypes showed moderate resistance (66.7%) to ciprofloxacin, sulfamethoxazole trimethoprim. The resistance genes including blaTEM, aadA1 and mphA were detected with a percentage of 100% in the six investigated isolates phenotypically resistant to ampicillin, gentamicin and erythromycin, respectively. The average count of E. coli serotype O157:H7 after 0.5-hour of dipping in essential oils (EOs) from oregano 2% (3.52 ±0.16) showed a significant decrease in comparison with that of the control. The average counts of E. coli serotype O157:H7 and reduction percentages after one hour of dipping in EOs from oregano 2% (3.41± 0.99, 48.4%); and in EOs from cinnamon 2% (3.74 ±0.13, 43.4%) showed a significant decrease when compared with that of the control. Our study clarified that the average counts of E. coli O157:H7 after one hour of dipping in EOs from oregano 2% and cinnamon 2% were significantly reduced when compared with those counts after dipping in EOs from oregano 1% and cinnamon 1%, respectively. The present study confirmed that cinnamon 2% and oregano 2% had powerful antibacterial activities against E. coli O175: H7 recovered from ready-to-eat (RTE) meat products and prevent food poisoning.

References

● 1. Paudyal N, Anihouvi V, Hounhouigan J, Matsheka MI, Sekwati-Monang B, Amoa-Awua W, Atter A, Ackah NB, Mbugua S, Asagbra A, Abdelga-dir W. Prevalence of foodborne pathogens in food from selected African countries–A meta–analysis. Int J Food Microbiol 2017 16;249:35–43.

● 2. Jiang X, Yu T, Wu N, Meng H, Shi L. Detection of qnr, aac (6′)–Ib–cr and qepA genes in Escherichia coli isolated from cooked meat products in Henan, China. Int J Food Microbiol. 2014;187:22–5.

● 3. 3.Yang S, Pei X, Wang G, Yan L, Hu J, Li Y, Li N, Yang D. Prevalence of food–borne pathogens in ready–to–eat meat products in seven different Chi-nese regions. Food Control. 2016;65:92–8

● 4. Zhao T, Doyle MP, Kemp MC, Howell RS, Zhao P. Influence of freezing and freezing plus acid-ic calcium sulfate and lacticacid addition on thermal inactivation of Escherichia coli O157: H7 in ground beef. J Food Prot. 2004;67(8):1760–4.

● 5. Ateba CN, Mbewe M. Detection of Escherichia coli O157: H7 virulence genes in isolates from beef, pork, water, human and animal species in the north-west province, South Africa: public health implica-tions. Res Microbiol 2011 1;162(3):240–8.

● 6. Geldreich, E.E. 1997 Coliforms: a new begin-ning to an old problem. In Coliforms and E. coli: Problem or Solution, eds. Kay, D. &Fricker, C. pp. 3–11. Cambridge: The Royal Society of Chemis-try.ISBN 0–85404–771–9

● 7. Hussein MA, Merwad AM, Elabbasy MT, Suelam II, Abdelwahab AM, Taha MA. Prevalence of Enterotoxigenic Staphylococcus aureus and Shiga Toxin Producing Escherichia coli in fish in Egypt: quality pa-rameters and public health hazard. Vector–Borne Zoonotic Dis. 2019;19(4):255–64.

● 8. Morshdy AE, Hussein MA, Tharwat AE, Moustafa NA, Hussein OK. Prevalence of shiga toxigenic and multi drug resistant Escherichia coli in ready to eat chicken products' sandwiches. Slov Vet Res. 2018 2;55.

● 9. Pitout JD, Laupland KB. Extended–spectrum β–lactamase–producing Enterobacteriaceae: an emerging public–health concern. The Lancet Inf Dis 2008;8(3):159–66.

● 10. Zhang S, Huang Y, Yang G, Lei T, Chen M, Ye Q, Wang J, Gu Q, Wei X, Zhang J, Wu Q. High prevalence of multidrug–resistant Escherichia coli and first detection of IncHI2/IncX4–plasmid carrying mcr–1 E. coli in retail ready–to–eat foods in China. Int J Food Microbiol 2021;355:109349.

● 11. Sabala RF, Usui M, Tamura Y, Abd–Elghany SM, Sallam KI, Elgazzar MM. Prevalence of colistin–resistant Escherichia coli harbouring mcr–1 in raw beef and ready–to–eat beef products in Egypt. Food Con-trol. 2021;119:107436.

● 12. Tadesse DA, Li C, Mukherjee S, Hsu CH, Bodeis Jones S, Gaines SA, Kabera C, Loneragan GH, Torrence M, Harhay DM, McDermott PF. Whole–genome sequence analysis of CTX–M con-taining Escherichia coli isolates from retail meats and cattle in the United States. Microbial Drug Re-sistance. 2018;24(7):939–48.

● 13. Spadafino JT, Cohen B, Liu J, Larson E. Tem-poral trends and risk factors for extended–spectrum beta–lactamase–producing Escherichia coli in adults with catheter–associated urinary tract infections. Antimicrobial resistance and infection control. 2014;3(1):1–4.

● 14. Dhillon RH, Clark J. ESBLs: a clear and pre-sent danger?. Critical care research and practice. 2012;2012.

● 15. Nazzaro F, Fratianni F, De Martino L, Coppola R, De Feo V. Effect of essential oils on pathogenic bacteria. Pharmaceuticals. 2013;6(12):1451–74.

● 16. Selim S. Antimicrobial activity of essential oils against Vancomycin–Resistant enterococci (VRE) and Escherichia coli O157: H7 in feta soft cheese and minced beef meat. Braz J Microbiol. 2011;42(1):187–96.

● 17. Mulani MS, Kamble EE, Kumkar SN, Tawre MS, Pardesi KR. Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial re-sistance: a review. Front Microbiol 2019;10:539.

● 18. Topić Popović N, Benussi Skukan A, Džidara P, Čož–Rakovac R, Strunjak–Perović I, Kozačinski L, Jadan M, Brlek–Gorski D. Microbiological quality of marketed fresh and frozen seafood caught off the Adriatic coast of Croatia. Vet Med 2010, 55(5), 233–241.

● 19. Cruickshank R, Duguid JR, Marmion BD, swain RHA. Medical Microbio The practice of Medi-cal Microbiology. VIII 11th and 12th Ed. Churchill Living Stone Edinberg, London and New York, USA; 1975.

● 20. Downes, F P., & Ito, K. Compendium of methods for the microbiological examination of foods Washington (676 p.). USA, 2001 American Public Health Association.

● 21. Khuntia, BK.. Basic Microbiology An illustrat-ed Laboratory Mannual.Daya Publishing house, 2011, New Delhi, India.

● 22. Cagney C, Crowley H, Duffy G, Sheridan JJ, O’brien S, Carney E, Anderson W, McDowell DA, Blair IS, Bishop RH. Prevalence and numbers of Escherichia coli O157: H7 in minced beef and beef burgers from butcher shops and supermarkets in the Republic of Ireland. Food Microbiol. 2004;21(2):203–12.

● 23. Kok T., Worswich D. & Gowans ESome sero-logical techniques for microbial and viral infections. In Practical Medical Microbiology (Collee J., Fraser A.,Marmion B. and Simmons A. eds.), 1996, 14 ed., Edinburgh, Churchill Livingstone, UK.

● 24. Bayer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol. 1966;45(4):493–6.

● 25. CLSL. Clinical and Laboratory Standards Insti-tute. Performance standards for antimicrobial suscep-tibility testing; sixteenth informational supplement. M100S16, Vol. 26, No. 3, Clinical and Laboratory Standards Institute 2016 Wayne, ennsylvania, 19087–1898, USA.

● 26. Mabilat C, Courvalin P. Development of" oli-gotyping" for characterization and molecular epide-miology of TEM beta–lactamases in members of the family Enterobacteriaceae. Antimicrob Agents Chemother. 1990;34(11):2210–6.

● 27. Randall LP, Cooles SW, Osborn MK, Piddock LJ, Woodward MJ. Antibiotic resistance genes, in-tegrons and multiple antibiotic resistance in thirty–five serotypes of Salmonella enterica isolated from hu-mans and animals in the UK. J Antimicrob Chemoth-er. 2004 ,53(2):208–16.

● 28. Nguyen MC, Woerther PL, Bouvet M, An-dremont A, Leclercq R, Canu A. Escherichia coli as reservoir for macrolide resistance genes. Emerg In-fect Dis 2009 ;15(10):1648.

● 29. Colom K, Pérez J, Alonso R, Fernández–Aranguiz A, Lariño E, Cisterna R. Simple and reliable multiplex PCR assay for detection of bla TEM, bla SHV and bla OXA–1 genes in Enterobacteriaceae. FEMS Microbiolo Lett. 2003;223(2):147–51.

● 30. Szczepanowski R, Linke B, Krahn I, Garte-mann KH, Guetzkow T, Eichler W, Pühler A, Schlueter A. Detection of 140 clinically relevant anti-biotic–resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing re-duced susceptibility to selected antibiotics. Microbiol 2009 155(7):2306–19.

● 31. Özkan G, Sağdiç O, Özcan M. Note: Inhibi-tion of pathogenic bacteria by essential oils at differ-ent concentrations. Food Sci Technol Int. 2003 9(2):85–8.

● 32. Al–Nabulsi A, Osaili T, Olaimat A, Almasri W, Al–Holy M, Jaradat Z, Ayyash M, Awaisheh S, Hol-ley R. Inhibitory effect of thyme and cinnamon es-sential oils against E. coli O157: H7 in Tahini. Food Sci Technol. 2020;40:885–93.

● 33. Osaili TM, Al–Nabulsi AA, Shaker RR, Al–Holy MM, Al–Haddaq MS, Olaimat AN, Ayyash MM, Al Ta'Ani MK, Forsythe SJ. Efficacy of the thin agar layer method for the recovery of stressed Crono-bacter spp.(Enterobacter sakazakii). J food Prot 2010;73(10):1913–8.

● 34. McHugh ML. The chi–square test of inde-pendence. Biochemia Medica. 2013;23(2):143–9.

● 35. Snedecor GW, Cochran WG. Statistical Meth-ods. 6th The Iowa St. Univ., Press. Amer., Iowa. USA pp. 1980:363–72.

● 36. Whyte P, McGill K, Monahan C, Collins JD. The effect of sampling time on the levels of micro–organisms recovered from broiler carcasses in a commercial slaughter plant. Food Microbiol. 2004;21 (1):59–65.

● 37. Hussein MA, Eldaly EA, Seadawy HG, El–Nagar EF. Virulence and antimicrobial resistance genes of Escherichia coli in ready to eat sandwiches in Sharkia Governorate. Slov Vet Res. 2018;55.

● 38. Shaltout FA, Farouk M, Ibrahim HA, Afifi ME. Incidence of E. coli and Salmonellae in ready to eat fast foods. Benha Vet Med J. 2017;32(1):18–22.

● 39. Karmi M. Escherichia coli O157: H7 in Raw and Processed Meat with Virulence Genes Detection in Aswan Governorate. Zag Vet J. 2019 1;47(3):259–66.

● 40. El–Dosoky HF, Shafik S, Baher M. Detection of spoilage and food poisoning bacteria in some ready to eat meat products in Dakahlia Governorate. Assiut Vet Med J 2013;59(138):71–8.

● 41. El–Bagory AM , Hassan Z, Amira Magdy A. Prevalence and Molecular Characterizations of Esche-richia coli in Meat Products. J Current Vet Res, 2020 (2), issue (1), 68–76.

● 42. Varman, A. H. and Evans, M.C. (1991): Food Borne pathogens. An illustrated text, chapter. 13, pp 267. England, Wolfe publishing Ltd. ISBN 07234, 1512,8.

● 43. Hassanien FS, El–Shater MA, El–Fatah A, Rabab R. Bacteriological aspect of meat and poultry meat meals. Benha Vet Med J. 2015;28(2):91–7.

● 44. Fayemi OE, Akanni GB, Elegbeleye JA, Abo-aba OO, Njage PM. Prevalence, characterization and antibiotic resistance of Shiga toxigenic Escherichia coli serogroups isolated from fresh beef and locally pro-cessed ready–to–eat meat products in Lagos, Nigeria. Int J Food Microbiol. 2021;347:109191.

● 45. Shilenge LB, Shale K, Matodzi T, Machete F, Tshelane C. A review of microbial hazards associated with meat processing in butcheries. Afr J Sci Techno Innov Developt. 2017;9(1):1–6.

● 46. El–Gazzar E, Hassanien F, Abou ELRoos NA. Bacterial hazards of ready to eat fish products. Benha Vet Med J. 2020;39(2):10–4.

● 47. Gupta B, Ghatak S, Gill JP. Incidence and virulence properties of E. coli isolated from fresh fish and ready–to–eat fish products. Vet World. 2013;6(1).

● 48. Hassanien FS, Shaltout FA, ELbaba AH, Adel NM. Microbiological evaluation of some heat treated fish products in Egyptian markets. Benha Vet Med J 2017;33(2):305–16.

● 49. Eldaly EA, Elshater MA, Hussein MA, Sharaf Eldin AM. Assessment of Food Poisoning Bacteria in Some Frozen Fish and Fish Products. Zag Vet J. 2015;43(3):46–52.

● 50. Karadal F, Onmaz NE, Hizlisoy H, Al SE, Telli N, Yildirim Y, Gonulalan Z. Isolation, genotyp-ing and antimicrobial susceptibility of pathogenic Escherichia coli serotypes in ready to eat foods. J Hell Vet Med Soc 2019;70(3):1661–8.

● 51. Olaleye ON, Abegunde TA. Microbiological safety assessment of selected smoked fish in Lagos Metropolis. Microbiolo Res J Int. 2015 29:1–5.

● 52. Hassanin FS, Reham AA, Shawky NA, Gomaa

WM. Incidence of Escherichia coli and Salmonella in Ready to eat Foods. Benha Vet Med J. 2014;27(1):84–91.

● 53. Grant MA, Hedberg C, Johnson R, Harris J, Logue CM, Meng J, Sofos JN, Dickson JS. The sig-nificance of non–O157 Shiga toxin–producing Esche-richia coli in food. Food Prot Trends. 2011;31(1):33–45.

● 54. Mellies JL, Barron AM, Carmona AM. Entero-pathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect Immun. 2007;75 (9): 4199–210.

● 55. Monaghan Á, Byrne B, Fanning S, Sweeney T, McDowell D, Bolton DJ. Serotypes and virulotypes of non–O157 shiga–toxin producing Escherichia coli (STEC) on bovine hides and carcasses. Food Micro-biol 2012;32(2):223–9.

● 56. Kochakkhani H, Dehghan P, Mousavi MH, Sarmadi B. Occurrence, molecular detection and antibiotic resistance profile of Escherichia coli O157: H7 isolated from ready–to–eat vegetable salads in Iran. Pharm Sci. 2016;22(3):195–202

● 57. Younis RI, Nasef SA, Salem WM. Detection of multi–drug resistant food–borne bacteria in ready–to–eat meat products in luxor city, Egypt. SVU.Int J Vet Sci. 2019;2(1):20–35.

● 58. Abass A, Adzitey F, Huda N. Escherichia coli of ready–to–eat (RTE) meats origin showed re-sistance to antibiotics used by farmers. Antibiotics. 2020;9(12):869.

● 59. Adzitey F, Ekli R, Aduah M. Incidence and antibiotic susceptibility of Staphylococcus aureus isolated from ready–to–eat meats in the environs of Bolga-tanga Municipality of Ghana. Cogent Environ Sci. 2020;6(1):1791463.

● 60. Zhao S, Blickenstaff K, Bodeis–Jones S, Gaines SA, Tong E, McDermott PF. Comparison of the prevalences and antimicrobial resistances of Esch-erichia coli isolates from different retail meats in the United States, 2002 to 2008. Appl Environ Microbiol. 2012;78(6):1701–7.

● 61. Gong S, Wang X, Yang Y, Bai L. Knowledge of food safety and handling in households: A survey of food handlers in Mainland China. Food Control. 2016 ;64:45–53.

● 62. Chantziaras I, Boyen F, Callens B, Dewulf J. Correlation between veterinary antimicrobial use and antimicrobial resistance in food–producing animals: a report on seven countries. J Antimicrob Chemother. 2014;69(3):827–34.

● 63. Altalhi AD, Gherbawy YA, Hassan SA. Anti-biotic resistance in Escherichia coli isolated from retail raw chicken meat in Taif, Saudi Arabia. Foodborne Pathog Dis 2010;7(3):281–5.

● 64. Hemeg HA. Molecular characterization of anti-biotic resistant Escherichia coli isolates recovered from food samples and outpatient Clinics, KSA. Sau-di J Biol Sci. 2018;25(5):928–31.

● 65. Vuthy Y, Lay KS, Seiha H, Kerleguer A, Ai-dara–Kane A. Antibiotic susceptibility and molecular characterization of resistance genes among Escherichia coli and among Salmonella subsp. in chicken food chains. Asian Pac J Trop Biomed. 2017;7(7):670–4.

● 66. 66. Abd El Tawab AA, El–Hofy FI, Khater DF, AL–Baaly YM. Molecular studies on toxigenic strains of Bacillus cereus isolated from some meat products. Benha Vet Med J. 2015;29(1):129–33.

● 67. Guo S, Tay MY, Aung KT, Seow KL, Ng LC, Purbojati RW, Drautz–Moses DI, Schuster SC, Schlundt J. Phenotypic and genotypic characteriza-tion of antimicrobial resistant Escherichia coli isolated from ready–to–eat food in Singapore using disk dif-fusion, broth microdilution and whole genome se-quencing methods. Food Control. 2019 ;99:89–97.

● 68. Amalaradjou MA, Baskaran SA, Ramanathan R, Johny AK, Charles AS, Valipe SR, Mattson T, Schreiber D, Juneja VK, Mancini R, Venkitana-rayanan K. Enhancing the thermal destruction of Escherichia coli O157: H7 in ground beef patties by trans–cinnamaldehyde. Food microbiol. 2010;27(6): 841–4.

● 69. Park, J. B., Kang, J. H., & Song, K. B. (2018). Antibacterial activities of a cinnamon essential oil with cetylpyridinium chloride emulsion against Esche-richia coli O157: H7 and Salmonella Typhimurium in basil leaves. Food Sci Biotechnol, 27(1), 47–55.

● 70. Osaili TM, Hasan F, Dhanasekaran DK, Obaid RS, Al–Nabulsi AA, Ayyash M, Karam L, Savvaidis IN, Holley R. Effect of active essential oils added to chicken tawook on the behaviour of Listeria monocyto-genes, Salmonella spp. and Escherichia coli O157: H7 dur-ing storage. Int J Food Microbiol. 2021;337:108947.

● 71. Chuesiang P, Sanguandeekul R, Siripatrawan U. Phase inversion temperature–fabricated cinnamon oil nanoemulsion as a natural preservative for prolonging shelf–life of chilled Asian seabass (Lates calcarifer) fillets. LWT. 2020;125:109122.

● 72. Chuesiang P, Siripatrawan U, Sanguandeekul R, Yang JS, McClements DJ, McLandsborough L. An-timicrobial activity and chemical stability of cinnamon oil in oil–in–water nanoemulsions fabricated using the phase inversion temperature method. LWT. 2019;110:190–6.

● 73. Lin L, Dai Y, Cui H. Antibacterial poly (eth-ylene oxide) electrospun nanofibers containing cin-namon essential oil/beta–cyclodextrin proteolipo-somes. Carbohydr polym. 2017 ;178:131–40.

● 74. Lambert RJ, Skandamis PN, Coote PJ, Nychas GJ. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J Appl Microbiol. 2001;91(3):453–62.

Downloads

Published

2021-12-17

How to Cite

Morshdy, A. E. M. A., Hussein, M. A., Merwad, A. M., El. Lawendy, H. M., Mohamed, A. H., & Saber, T. (2021). INCIDENCE AND CHARACTERIZATION OF ANTIMICROBIAL RESISTANCE OF Escherichia coli IN FAST FOOD WITH SPECIAL REFERENCE TO THE ANTIBACTERIAL EFFECTS OF CINNAMON AND OREGANO ESSENTIAL OILS AGAINST E. coli O157:H7 IN MINCED MEAT. Slovenian Veterinary Research, 58(24-Suppl), 389–401. https://doi.org/10.26873/SVR-1458-2021

Issue

Section

Original Research Article

Most read articles by the same author(s)