| More

Isolation, genotyping and antimicrobial susceptibility of pathogenic Escherichia coli serotypes in ready to eat foods

Views: 700 Downloads: 399
F. KARADAL, N. ERTAS ONMAZ, H. HIZLISOY, S. AL, N. TELLI, Y. YILDIRIM, Z. GONULALAN
F. KARADAL, N. ERTAS ONMAZ, H. HIZLISOY, S. AL, N. TELLI, Y. YILDIRIM, Z. GONULALAN

Abstract


In this study, pathogenic Escherichia coli serotypes (E. coli O157:H7, O26, O111) and their molecular proximity and antimicrobial susceptibility were investigated in RTE foods. A total of 240 samples; consist of 105 stuffed mussel, 56 meatless cig kofte, 54 Russian salad, 25 cheese halva, were analyzed. The conventional culture and serotyping methods for determination of the organisms were performed and further confirmation by PCR was carried out. Confirmed E. coli O157 isolates were genotyped by the enterobacterial repetitive intergenic consensus

(ERIC)-PCR. Antibacterial susceptibility testing of the isolates was performed by disc diffusion method. E. coli was detected in 7 (2.9 %) of 240 samples, including 3 (5.5%) Russian salad, 3 (2.8%) stuffed mussel, 1 (4 %) cheese halva. Two isolates from Russian salad, 1 from stuffed mussel and 1 from cheese halva were identified as E. coli O157 . In addition, stuffed mussel isolate was found to carry stx1 ve hlyA genes whereas one Russian salad isolate carried the stx1 gene. E. coli isolates were found to be resistant to amoxycillin/clavulonic acid, gentamicin and ciprofloxacin, at the rate of 29%, 14% and 29 %, respectively. Only one (14 %) isolate from stuffed mussel was classified as multidrug resistant to three antimicrobials. Furthermore, the isolates, related to O157 and O157:H7, presented different ribotypes in this study. The results provide useful data for the development of public health policy concerning the potential presence of pathogenic antimicrobial resistant E. coli serotypes in RTE foods. Strict surveillance of RTE foods at retail points for emerging pathogens, their antimicrobial resistance patterns and the potential likelihood of cross-contamination is required.

Keywords


Antimicrobial susceptibility; cheese halva; ERIC-PCR; meatless cig kofte; Russian salad; EHEC; stuffed mussel.

Full Text:

PDF

References


Ates M, Ozkizilcik A, Tabakoglu C (2011) Microbiological analysis of stuffed mussels sold in the streets. Indian J Med Microbiol 51(3):350-354.

Baloch AB, Yang H, Feng Y, Xi M, Wu Q, Yang Q, Tang J, He X, Xiao Y, Xia X (2017) Presence and Antimicrobial resistance of Escherichia coli in Ready-to-Eat Foods in Shaanxi, China. J Food Prot 80(3):420-424.

Bingol EB, Colak H, Hampikyan H, Muratoglu K (2008) The microbiological quality of stuffed mussels (Midye Dolma) sold in Istanbul. Brit Food J 110(11):1079-1087.

Bruyand M, Mariani-Kurkdjian P, Gouali M, de Valk H, King LA, Hello SL, Bonacorsi S, Loirat C (2018) Hemolytic uremic syndrome due to Shiga toxin-producing Escherichia coli infection. Med Mal Infect 48:167-174.

Campos J, Mourao J, Pestana N, Peixe L, Novais C, Antunes P (2013). Microbiological quality of ready-to-eat salads: an underestimated vehicle of bacteria and clinically relevant antibiotic resistance genes. Int J Food Microbiol, 166 (3), 464–470.

Chapman PA, Wright DJ, Siddons CA (1996) A comparison of immunomagnetic separation and direct culture for the isolation of verocytotoxin-producing Escherichia coli O157 from bovine faeces. J Med Microbiol 40:424–427.

Cho JI, Cheung CY, Lee SM, Ko S I, Kim K H, Hwang IS, Kim SH, Cho SY, Lim CJ, Lee KH, Ha SD, Kim KS (2011) Assessment of microbial contamination levels of street- vended foods in Korea. J. Food Safety, 31: 41-47.

Clermont O, Lescat M, O’Brien LC, Gordon DM, Tenaillon O, Denamur E (2008) Evidence for a human-specific Escherichia coli clone. Environ Microbiol 10:1000–1006.

Cody SH, Glynn MK, Farrar JA, Cairns KL, Griffin PM, Kobayashi J, et al. (1999) An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Ann Intern Med 130:202-209.

Cokal Y, Dagdelen A, Cenet O, Gunsen U (2012) Presence of L. monocytogenes and some bacterial pathogens in two Turkish traditional foods, Mihalic cheese and Hosmerim dessert. Food Contol 26:337-340.

Delikanli B, Sonmez B, Ozdemir Y (2014) Microbiological quality of the meat-free cig kofte consumed in Bursa City center. Harran Univ J Fac Vet Med 3(1):13-17.

Dontorou A, Papadopoulou C, Filioussis G, Economou V, Apostolou I, Zakkas G, Salamoura A, Kansouzidou A, Levidiotou S (2003) Isolation of Escherichia coli O157:H7 from foods in Greece. Int J Food Microbiol 82: 273-279.

Durso LM Bono JL Keen JE (2005) Molecular serotyping of Escherichia coli O26:H11. Appl Environ Microbiol 71:4941–4944.

Elobeid T, Aziz HA, Mousa R, Alzahiri A (2014) Survey on the microbial quality of traditional foods sold by street vendors in Qatar. Austin J NutrMetab 1(2): 4-20.

Fratamico PM, Bagi LK, Pepe TA (2000) multiplex polymerase chain reaction assay for rapid detection and identification of Escherichia coli O157:H7 in foods and bovine feces. J Food Protect 63:1032-1037.

Gourmelon M, Montet MP, Lozach S, Le Mennec C, Pommepuy M, Beutin L, Vernozy-Rozand C (2006) First isolation of Shiga toxin 1d producing Escherichia coli variant strains in shellfish from coastal areas in France. J Appl Microbiol 100: 85-97.

Gupta B, Ghatak S, Gill JPS (2013) Incidence and virulence properties of E. coli isolated from fresh fish and ready-to-eat fish products. Vet. World 6(1): 5-9.

Hampikyan H, Ulusoy B, Bingöl EB, Çolak H, Akhan M (2008) Determination of microbiological quality of some grilled food, salad and appetizers. Türk Mikrobiol Soc 38:87–94 (article in Turkish with an abstract in English).

Hassanin FS, Reham A, Amin, Shawky NA, Gomaa WM (2014) Incidence of Escherichia coli and Salmonella in ready to eat foods. Benha Veterinary Medical Journal 27(1): 84-91.

Houf KL, De Zutter L, Van Hoof J, Vandamme P (2002) Assessment of the genetic diversity among arcobacters isolated from poultry products by using two PCR-based typing methods. Appl Environ Microbiol 68:2172–2178.

Jaroni D, Ravishankar S, Juneya V (2010) Chapter 1: Microbiology of ready-to-eat foods. In: Hwang A. and Huang L (Eds), Ready-to-Eat Foods Microbial Concerns and Control Measures. Boca Raton: CRC Press, pp.1-60.

Karlowsky JA, Kelly LJ, Thornsberry C, Jones ME Sahm DF (2002) Trends in antimicrobial resistance among urinary tract infection isolates of Escherichia coli from female outpatients in the United States. Antimicrob. Agents Chemother 46: 2540–2545.

Kim JS, Kim Y (2007) The inhibitory effect of natural bioactives on the growth of pathogenic bacteria. Nutr Res Pract 1: 273-278.

Kisla D, Uzgun Y (2008) Microbiological evaluation of stuffed mussels. JPF 7:616–620.

Koidis P, Iossifidou E, Abrahim A, Ambrosiadis I (2000) The effectiveness of different spices as inhibitors for Escherichia coli O157:H7 in nutrient broth stored at 4°C or 12°C. Arch. Lebensmittelhyg 51 (6):129 – 152.

Kocatepe D, Taşkaya G, Turan H Kaya Y (2016) Microbiological investigation of wild, cultivated mussles (Mytilus galloprovincialis L. 1819) and stuffed mussels in Sinop Turkey. Ukranian Food Journal 5 (2):299-305.

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

Lima CM, Souza IEGL, Dos Santos Alves T, Leite CC, Evangelista-Barreto NS, de Castro Almeida RC (2017) Antimicrobial resistance in diarrheagenic Escherichia coli from ready-to-eat foods. J Food Sci Technol 54:3612–3619.

Lynch MJ, O’Connor L, Fox EM, Jordan K, Murphy M (2012) Verocytotoxigenic Escherichia coli O157, O111, O26, O103, O145 in Irish dairy cattle and raw milk: prevalence and epidemiology of emergent stains. Zoonoses Public Hlth 59: 264–271.

Maurer JJ, Schmidt D, Petrosko P, Sanchez S, Bolton L, Lee MD (1999). Development of primers to O-antigen biosynthesis genes for specific detection of Escherichia coli O157 by PCR. Appl Environ Microbiol 65: 2954-2960.

Montville TJ, Matthews KR, Kniel KE (2012) Food Microbiology an Introduction, In: Chapter 12, Enterohemorrhagic Escherichia coli. Washington, USA: ASM Press, 3rd Edition, p.170-87.

Obrig TG (2010) Escherichia coli shiga toxin mechanisms of action in renal disease. Toxins 2: 2769–2794.

Oz V, Karadayi S, Cakan H, Karadayi B, Cevik FE (2014) Assessment of microbiological quality of ready-to-eat foods in Istanbul, Turkey J Food Agric Environ 12:56-60.

Paton AW, Paton JC (1998) Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. J Clin Microbiol 36:598–602.

Prakasan S, Prabhakar P, Lekshmi M, Nayak BB, Kumar S (2018) Isolation of Shiga toxin-producing Escherichia coli harboring variant Shiga toxin genes from seafood. Vet World 11: 379-385.

Rasheed MU, Thajuddin N, Ahamed P, Teklemariam Z, Jamil K (2014) Antimicrobial drug resistance in strains of Escherichia coli isolated from food sources. Rev Inst Med Trop Sao Paulo 56(4):341–346.

Rounds L, Havens CM, Feinstein Y, Friedman M, Ravishankar S (2013) Concentration-dependent inhibition of Escherichia coli O157:H7 and heterocyclic amines in heated ground beef patties by apple and olive extracts, onion powder and clove bud oil. Meat Sci 94(4):461-467.

Sarimehmetoglu B, Aksoy MH, Ayaz ND, Ayaz Y, Kuplulu O, Kaplan YZ (2009). Detection of Escherichia coli O157:H7 in ground beef using immunomagnetic separation and multiplex PCR. Food Control 20: 357-361.

Secim Y, Ucar G (2017) Evaluation of the desserts; which are hosmerim, cheese halva, kunafah produced in Turkish cuisine -in aspect of tourism. IJSSER 3(5): 1478-1484.

Sengor GF, Kalafatoğlu H, Gun H (2004) The determination of microbial flora, water activity and chemical analyses in smoked, canned mussels (Mytilus galloprovincialis, L.). Turk J Vet Anim Sci 28: 793-797.

Spencer KC (2005) Chapter 12: Modified atmosphere packaging of readyto-eat foods. In: Han J.H. (ed) Innovations in food packaging. Elsevier, USA, pp. 185-203.

Surendraraj A, Thampuran N, Joseph TC (2010) Molecular screening, isolation, and characterization of enterohemorrhagic Escherichia coli O157:H7 from retail shrimp J Food Protec 73 (1): 97–103.

Taban MB (2012) Listeria monocytogenes in cig kofte without meat: A novel bulgur ball product. J Food Agric Environ 10(2): 130-132.

Tudoran AA, Fischer ARH, van Trijp HCM, Grunert K, Krystallis A, Esbjerg L (2012) Overview of consumer trends in food industry, retailer and consumer acceptance of promising novel technologies and collaborative innovation management, Retailer and Consumer Acceptance of Promising Novel Technologies and Collaborative Innovation Management, Deliverable D2.1 p.8.

Wahi S, Bansal S, Ghosh M, Ganguli A (2006) Growth and survival of Escherichia coli O157:H7 during manufacture and storage of Indian cheese (paneer). Foodborne Pathog Dis 3(2):184-189.

Ye Q, Wu Q, Zhang S, Zhang J, Yang G, Wang J, Xue L and Chen M (2018). Characterization of Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae from retail food in China. Front Microbiol 9: 1-12.

Zhao T, Doyle MP (1993) Fate of Enterohemorrhagic Escherichia coli 0157: H7 in commercial mayonnaise. J Food Prot 57: 780-783.

Zweifel C, Giezendanner N, Corti S, Krause G, Beutin L, Danuser J, Stephan R (2010) Characteristics of Shiga toxin-producing Escherichia coli isolated from Swiss raw milk cheese within a 3-year monitoring program. J Food Prot 73: 88–91.


Refbacks

  • There are currently no refbacks.


Copyright (c) 2019 F. KARADAL, N. ERTAS ONMAZ, H. HIZLISOY, S. AL, N. TELLI, Y. YILDIRIM, Z. GONULALAN

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