Molecular characterization of çig köfte sold at retail in Ankara, Turkey, and evaluation of selected antimicrobials as ingredients to control foodborne pathogens in çig köfte during refrigerated storage

Authors: GHAZZI, MARYA - University Of Michigan; Porto-Fett, Anna; AYAS, NAIM - Kirikkale University; OZANSOY, GORKEM - Ankara University Of Turkey; CUFAOGLU, GIZEM - Ankara University Of Turkey; GONCUOGLU, MUAMMER - Ankara University Of Turkey; DLUZNESKI, ASHTON - Pennsylvania State University; HOLINKA, SARINA - University Of Colorado; Shoyer, Brad; Shane, Laura; STAHLER, LAURA - Former ARS Employee; CAMPANO, STEPHEN - Hawkins, Inc; Luchansky, John

Submitted to: Food Control
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/21/2017
Publication Date: 8/3/2017
Citation: Ghazzi, M., Porto Fett, A.C., Ayas, N.D., Ozansoy, G., Cufaoglu, G., Goncuoglu, M., Dluzneski, A., Holinka, S., Shoyer, B.A., Shane, L.E., Stahler, L., Campano, S., Luchansky, J.B. 2018. Molecular characterization of çig köfte sold at retail in Ankara, Turkey, and evaluation of selected antimicrobials as ingredients to control foodborne pathogens in çig köfte during refrigerated storage. Food Control. 84:138-147.

Interpretive Summary: Cig kofte (translated as “raw meatball”) is a traditional Turkish raw meat product prepared and consumed as fresh and without further processing. It is usually prepared with lean raw ground beef, fine bulgur wheat, and a wide array of spices such as salt, paprika, cumin, red pepper paste, tomato paste, red and black pepper, onion, and garlic. Consumption of tartare-type, ready-to-eat beef products, such as cig kofte, are potentially risky due to the potential presence and possible survival/growth of foodborne pathogens in such products. Food market surveys have demonstrated that the microbiological quality of cig kofte at Turkish retail markets can be generally unsatisfactory, mostly due to lack of hygiene during handling/preparation of the product, lack of temperature control during storage, and/or poor quality of the ingredients used. In fact, we were able to recover pathogenic strains of Listeria monocytogenes, Salmonella, and E. coli in a survey of cig kofte from eateries and markets in Turkey. For these reasons, we evaluated the effect of including vinegar as an ingredient for cig kofte to control pathogenic cells of Shiga toxin-producing E.coli, Salmonella, and Listeria monocytogenes. In the absence of spices and vinegar and during storage at an abusive temperature such as 15 degree Celsius, pathogen growth was not suppressed. In contrast, inclusion of spices and vinegar in the formulation of cig kofte inhibited outgrowth of all three pathogens at both refrigeration and abusive temperatures, thus lowering the likelihood for pathogen presence/persistence and enhancing product safety.

Technical Abstract: We surveyed cig kofte purchased from restaurants or retail establishments in Turkey and monitored viability of Shiga toxin-producing Escherichia coli (STEC), Salmonella spp., or Listeria monocytogenes inoculated into cig kofte formulated with buffered or distilled vinegar in our laboratory. Regarding the former, of the 24 beef and 144 meatless samples of cig kofte tested, Salmonella was only recovered from the meatless samples (1 of 24 samples; detection limit was <2.3 log CFU/g). L. monocytogenes was recovered from 2 of 24 beef (8.3%) and 2 of 144 non-meat (1.4%) samples of cig kofte, whereas E. coli O157 was recovered from 5 of 24 meat (20.8%) and 21 of 144 non-meat (14.6%) of cig kofte tested. For the inoculated product study, finely-ground beef (93:7%, lean:fat) was separately inoculated (ca. 4.0 log CFU/g) with an eight-strain cocktail of STEC or a five-strain cocktail of Salmonella spp. or L. monocytogenes and then mixed with either bulgur wheat alone or with bulgur wheat along with salt, tomato sauce, diced tomatoes, green peppers, onion powder, fresh garlic cloves, and various spices. Next, aliquots of buffered vinegar (BV) or distilled white vinegar (DV; 5% acidity) were added to the inoculated batter to deliver 0.0, 2.5, or 5.0% (vol/wt) of the antimicrobial. The resultant batter was shaped into ca. 15 g balls by hand and stored at 4 deg or 15 deg C for up to 3 days. When cig kofte was formulated with or without spices and with or without antimicrobials, STEC, Salmonella spp., and L. monocytogenes numbers remained relatively unchanged after 3 days of storage at 4 deg C. In contrast, when cig kofte was formulated without spices and without antimicrobials, STEC, Salmonella spp., and L. monocytogenes levels increased by ca. 0.2 to 0.9 log CFU/g, respectively, after 3 days at 15 deg C. When product was formulated with spices, in the absence of antimicrobials, STEC and L. monocytogenes levels decreased by ca. 0.3 and 0.7 log CFU/g respectively, whereas Salmonella spp. increased by ca. 0.3 log CFU/g. The formulation of cig kofte used in this study did not support growth of either STEC or L. monocytogenes. Our data also highlight the antimicrobial contributions of the spice mix used for cig kofte and the importance of proper handling and storage practices to ensure its safety.