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Investigation of efficient thermal inactivation parameters of Escherichia coli O157:H7 in meatballs by grilling

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Abstract

The aim of the study was to investigate the safe cooking parameters to eliminate E.coli O157:H7 in commonly consumed meatball types, by simulating the meatball formula and the cooking practices of restaurants. Ground meat was inoculated around 7 ± 1 log cfu/g with a cocktail of 5 strains of E.coli O157:H7. The meatballs were prepared with different ingredients and seasonings depending on the type (kasap or İnegöl). The cooking experiments were conducted on a grill, at two different temperatures, 170 and 180 °C. Results show that, in order to achieve ≥ 5 log destruction of E.coli O157:H7 in Kasap and İnegöl meatballs cooked at 170 °C, the internal temperature should reach to 85 °C. On the other hand, when the meatballs were grilled at 180 °C, 5 log reductions were achieved by cooking the meatballs to an internal temperature of 80 °C for Kasap meatballs and 85 °C for İnegöl meatballs. Differences in the meatball formulation and shape affected the thermal destruction of E.coli O157:H7. Measuring of the grill temperature and core temperature of meatballs during cooking and reaching the target temperatures for each type of meatball would help prevent Shiga toxin-producing E.coli (STEC) infections in public eating establishments.

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Data availability statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

Not applicable.

Abbreviations

E. coli:

Escherichia coli

STEC:

Shiga toxin-producing E. coli

USDA:

U.S. Department of Agriculture

FSIS:

Food safety and inspection service

ATCC:

American Type Culture Collection

RSKK:

Refik saydam culture collection

PBS:

Phosphate buffered saline

SMAC:

Sorbitol MacConkey Agar

GLM:

General linear models

SAS:

Statistical analysis system

References

  • AOAC (1990) Official methods of analysis, 15th edn. Association of Official Analytical Chemists, Washington

    Google Scholar 

  • Byrne CM, Bolton DJ, Sheridan JJ, Blair IS, McDowell DA (2002) The effect of commercial production and product formulation stresses on the heat resistance of Escherichia coli O157: H7 (NCTC 12900) in beef burgers. Int J Food Microbiol 79(3):183–192

    Article  CAS  PubMed  Google Scholar 

  • Centers for Disease Control and Prevention (CDC) (2014) Infections linked to ground beef. https://www.cdc.gov/ecoli/2014/O157H7-05-14/index.html. Accessed 18 Nov 2020

  • Centers for Disease Control and Prevention (CDC) (2019) Outbreak of E.coli infections linked to ground beef. https://www.cdc.gov/ecoli/2019/o103-04-19/index.html. Accessed 18 Nov 2020

  • Çalıcıoğlu M, Ateş G, İlhak İ, Bozkurt P, Şeker P, Dikici A (2006) Kıymalı pide üretim koşullarının Salmonella, Listeria monocytogenes ve Escherichia coli O157:H7 patojenlerinin inaktivasyonu üzerine etkisi. Tübitak, 2006-198.

  • Dhaliwal HK, Gänzle M, Roopesh MS (2021) Influence of drying conditions, food composition, and water activity on the thermal resistance of Salmonella enterica. Food Res Int 147:110548

    Article  CAS  PubMed  Google Scholar 

  • Direkel Ş, Yıldız Ç, Aydın F, Emekdaş G (2010) Mersin İli Yenişehir İlçesi\'nde Satışa Sunulan Çiğ Kıymaların Mikrobiyolojik Kalitesinin Değerlendirilmesi (Evaluation of microbiological quality of ground meat marketed in Yenisehir County, Mersin Province). Mersin Üniver Sağlık Bilim Derg (Mersin Univer J Health Sci) 3(2):8–14. https://dergipark.org.tr/tr/pub/mersinsbd/issue/19524/207925

  • Gilbert S, McIntyre L, Lake R, Wong TL, Hudson JA, Olsen L, Cook RL (2011) Background document on factors influencing the heat inactivation of bacteria in foods. Ministry for Primary Industries, MPI Technical Paper No: 2016/08

  • Gökalp HY, Kaya M, Tülek Y, Zorba Ö (1993) Et ve et ürünlerinde kalite kontrolü ve laboratuvar uygulama klavuzu. Atatürk University Publication No: 751, Faculty of Agriculture Publications No: 318. Textbooks Series No: 69. Atatürk University Faculty of Agriculture Offset Facility. Erzurum, p 287

  • Kalender H (2013) Isolation, virulence genes and antimicrobial susceptibilities of Shiga Toxinproducing Escherichia coli O157 from slaughtered cattle in Abattoirs and ground beef Sold in Elazığ. Kafkas Univ Vet Fak Derg 19(3):461–467

    Google Scholar 

  • Kök F, Sezgin E (2015) Aydın’da Tüketime Sunulan Kıyma Ve Hamburger Köftelerde Escherichia coli O157:H7 Varlığının Araştırılması. MJEN 3(1):58–69. https://dergipark.org.tr/tr/pub/mjen/issue/40442/48431

  • Lahou E, Wang X, De Boeck E, Verguldt E, Geeraerd A, Devlieghere F, Uyttendaele M (2015) Effectiveness of inactivation of foodborne pathogens during simulated home pan frying of steak, hamburger or meat strips. Int J Food Microbiol 206:118–129. https://doi.org/10.1016/j.ijfoodmicro.2015.04.014

    Article  PubMed  Google Scholar 

  • Li KW, McKeith AG, Shen C, McKeith R (2018) A comparison study of quality attributes of ground beef and veal patties and thermal inactivation of Escherichia coli O157:H7 after double pan-broiling under dynamic conditions. Foods 7(1):1–13. https://doi.org/10.3390/foods7010001

    Article  CAS  Google Scholar 

  • Luchansky JB, Porto-Fett ACS, Shoyer BA, Phillips J, Chen V, Eblen DR, Cook LV, Mohr TB, Esteben E, Bauer N (2013) Fate of Shiga toxin-producing O157:H7 and non-O157:H7 Escherichia coli cells within refrigerated, frozen, or frozen then thawed ground beef patties cooked on a commercial open-flame gas or a clamshell electric grill. J Food Prot 76(9):1500–1512. https://doi.org/10.4315/0362-028X.JFP-12-432

    Article  PubMed  Google Scholar 

  • Manios SG, Skandamis PN (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 Sci 101:25–32. https://doi.org/10.1016/j.meatsci.2014.10.031

    Article  CAS  PubMed  Google Scholar 

  • Nair MS, Lau P, Belskie K, Fancher S, Chen CH, Karumathil DP, Venkitanarayanan K (2016) Potentiating the heat inactivation of Escherichia coli O157:H7 in ground beef patties by natural antimicrobials. Front Microbiol 7:1–8. https://doi.org/10.3389/fmicb.2016.00015

    Article  Google Scholar 

  • Osaili T, Griffis CL, Martin EM, Beard BL, Keener A, Marcy JA (2006) Thermal inactivation studies of Escherichia coli O157: H7, Salmonella, and Listeria monocytogenes in ready-to-eat chicken-fried beef patties. J Food Prot 69(5):1080–1086

    Article  CAS  PubMed  Google Scholar 

  • Oteiza JM, Giannuzzi L, Califano AN (2003) Thermal inactivation of Escherichia coli O157: H7 and Escherichia coli isolated from morcilla as affected by composition of the product. Food Res Int 36(7):703–712

    Article  Google Scholar 

  • Park S, Worobo R, Durst R (2010) Escherichia coli O157:H7 as an emerging foodborne pathogen: a literature review. Crit Rev Food Sci Nutr 39(6):481–502. https://doi.org/10.1080/07388551.2001.10446386

    Article  Google Scholar 

  • Porto-Fett ACS, Oliver M, Daniel M, Shoyer BA, Stahler LJ, Shane LE, Luchansky JB (2016) Effect of deep-frying or conventional oven cooking on thermal inactivation of Shiga toxin-producing cells of Escherichia coli in meatballs. J Food Prot 79(5):723–731. https://doi.org/10.4315/0362-028X.JFP-15-427

    Article  CAS  PubMed  Google Scholar 

  • Statistical Analyses System (SAS) (1999) Version 8. SAS Institute Inc., Cary, NC, USA

  • Shen C, Geornaras I, Belk KE, Smith GC, Sofos JN (2011a) Thermal inactivation of acid, cold, heat, starvation, and desiccation stress-adapted Escherichia coli O157:H7 in moisture-enhanced non-intact beef. J Food Prot 74(4):531–538. https://doi.org/10.4315/0362-028X.JFP-10-430

    Article  PubMed  Google Scholar 

  • Shen C, Geornaras I, Belk KE, Smith GC, Sofos JN (2011b) Inactivation of Escherichia coli O157:H7 in moisture-enhanced non-intact beef by pan-broiling or roasting with various cooking appliances set at different temperatures. J Food Sci 76(1):64–71. https://doi.org/10.1111/j.1750-3841.2010.01882.x

    Article  Google Scholar 

  • Sofos JN, Geornaras I (2010) Overview of current meat hygiene and safety risks and summary of recent studies on biofilms, and control of Escherichia coli O157: H7 in nonintact, and Listeria monocytogenes in ready-to-eat, meat products. Meat Sci 86(1):2–14. https://doi.org/10.1016/j.meatsci.2010.04.015

    Article  PubMed  Google Scholar 

  • Turkish Standardization Institute (TSE) 3136 (1978) Et ve et mamüllerinde pH Tayini (Determination of pH in meat and meat products). Turkish Standardization Institute, Ankara

  • USDA (2012) United States Department of Agriculture, Food Safety and Inspection Service (2012) USDA Targeting Six Additional Strains of E.coli in Raw Beef Trim Starting Monday. https://www.usda.gov/media/press‐releases/2012/05/31/usda‐targeting‐six‐additional‐strains‐ecoli‐rawbeef‐trim‐starting. Accessed 20 Jun 20

  • USDA (2017) United States Department of Agriculture, Food Safety and Inspection Service Marcho Farms, Inc. Recalls Veal, Beef and Pork Products due to Possible non-O157 Shiga Toxin-Producing E. coli (STEC) Adulteration. https://www.fsis.usda.gov/recalls-alerts/majestic-meat-company-recalls-ground-beef-products-due-possible-e.-coli-o157h7. Accessed 28 Nov 2021

  • USDA (2018a) United States Department of Agriculture, Food Safety and Inspection Service Cargill Meat Solutions Recalls Ground Beef Products due to Possible E. coli O26 Contamination. https://www.fsis.usda.gov/wps/portal/fsis/topics/recalls-and-public-health-alerts/recall-case-archive/archive/2018/recall-081-2018-release. Accessed 28 Nov 2021

  • USDA (2018b) United States Department of Agriculture, Food Safety and Inspection Service Majestic Meat Company Recalls Ground Beef Products due to Possible E. coli O157:H7 Contamination. https://www.fsis.usda.gov/wps/portal/fsis/topics/recalls-and-public-health-alerts/recall-case-archive/archive/2018/recall-113-2018-release. Accessed 28 Nov 2021

  • USDA (2020) United States Department of Agriculture Food Safety and Inspection Service. Safe minimum internal temperature chart. https://www.fsis.usda.gov/safetempchart. Accessed 28 May 2020

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Authors and Affiliations

  1. Department of Food Engineering, Faculty of Engineering, Uşak University, Uşak, Turkey

    Özge Tosuncuk & Abdullah Dikici

  2. Department of Food Engineering, Faculty of Engineering, Manisa Celal Bayar University, Manisa, Turkey

    S. Betül Bozatli

  3. Gıda Mühendisliği Bölümü, Mühendislik Fakültesi, Uşak Üniversitesi, Ankara İzmir Yolu 8.Km 1.Eylül Kampüsü, Uşak, Turkey

    Abdullah Dikici

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  1. Özge Tosuncuk
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  2. S. Betül Bozatli
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  3. Abdullah Dikici
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Contributions

AD, responsible for conceiving the idea, supervised the work, edited the manuscript. SBB wrote the manuscript. OT and SBB carried out the experiments. OT performed statistical analysis. AD, SBB and OT revised the manuscript.

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Correspondence to Abdullah Dikici.

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Tosuncuk, Ö., Bozatli, S.B. & Dikici, A. Investigation of efficient thermal inactivation parameters of Escherichia coli O157:H7 in meatballs by grilling. J Food Sci Technol 60, 1731–1737 (2023). https://doi.org/10.1007/s13197-023-05710-6

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  • DOI: https://doi.org/10.1007/s13197-023-05710-6

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