Prevalence and Antibiotic Resistance of Salmonella Spp., E. Coli O157, and L. Monocytogenes in Meat and Dairy Products

Yıl 2021, Cilt: 10 Sayı: 1, 17 - 22, 11.06.2021

Can Atabey Tolga Kahraman Ahmet Koluman

Öz

Bacteria-related food poisoning is the most prevalent cause of food borne diseases, reaching up to 33 percent of the incidents. The study aimed to provide data for the risk assessment processes focusing on poisoning due to the consumption of foods of animal origin.
Bovine meat, drumstick and breast chicken meat, white cheese, and cheddar samples were collected from five different stores in Tekirdağ, Turkey, monthly for twelve consecutive months, from January 1 to December 31, 2019.
Results showed that 4,16% of the samples (n=22) were contaminated with Salmonella sp. (n=12), Escherichia coli O157 (n=4), and Listeria monocytogenes (n=6). Antibiotic sensitivity studies revealed that the microorganisms were resistant to 8 different antibiotics.
Despite the low number of pathogens isolated, their presences with the high antibiotic resistance rates pose a significant threat to public health.

Anahtar Kelimeler

antibiotic resistance, e.coli O157, salmonella sp., l.monocytogenes

Proje Numarası

TDK-201831189

Kaynakça

• Acaröz, U., Gurler, Z., Kara, R., Arslan-Acaröz, D., & Zemheri, F. (2018). Afyonkarahisar İlinde Satışa Sunulan Tavuk Eti ve Sakatatlarında Salmonella spp. Varlığının Belirlenmesi. Kocatepe Veterinary Journal, 1–5. https://doi.org/10.30607/kvj.444137
• Ahmed, A. M., & Shimamoto, T. (2014). Isolation and molecular characterization of Salmonella enterica, Escherichia coli O157:H7 and Shigella spp. From meat and dairy products in Egypt. International Journal of Food Microbiology, 168–169, 57–62. https://doi.org/10.1016/j.ijfoodmicro.2013.10.014
• Akkaya, L., & Alişarlı, M. (2006). Afyonkarahisar’da Tüketime Sunulan Peynirlerde Listeria monocytogenes ve Salmonella spp. Varlığının Belirlenmesi. Yüzüncü Yıl Üniversitesi Veteriner Fakültesi Dergisi, 17(1–2), 87–91.
• Akkaya, L., Alişarlı, M., Kara, R., & Telli, R. (2007). Afyonkarahisar’da Tüketime Sunulan Çig Süt ve Peynirlerde E. coli O157:H7 Varlığının Belirlenmesi. YYÜ VET FAK DERG, 18(1), 1–5.
• Alonso-Hernando, A., Prieto, M., García-Fernández, C., Alonso-Calleja, C., & Capita, R. (2012). Increase over time in the prevalence of multiple antibiotic resistance among isolates of Listeria monocytogenes from poultry in Spain. Food Control, 23(1), 37–41. https://doi.org/10.1016/j.foodcont.2011.06.006
• Arslan, S., & Özdemir, F. (2008). Prevalence and antimicrobial resistance of Listeria spp. In homemade white cheese. Food Control, 19, 360–363.
• Atabey, C. (2011). Piyasada Satışa Sunulan Peynirlerden Elde Edilen Jenerik Escherichia coli Ve Staphylococcus Aureus Suşlarının Antibiyotik Dirençliliklerinin Belirlenerek, Mastitis Kontrol Ve Tedavi Programlarında Kullanılan Antibiyotiklerle İlişkisinin Belirlenmesi. [Yüksek Lisans Tezi]. Adnan Menderes Üniversitesi Sağlık Bilimleri Enstitüsü.
• Aygun, O., & Pehlivanlar, S. (2006). Listeria spp. In the raw milk and dairy products in Antakya, Turkey. Food Control, 17(8), 676–679. https://doi.org/10.1016/j.foodcont.2005.09.014
• Berktaş, M., Bozkurt, E. N., Bozkurt, H., Alişarlı, M., & Güdücüoğlu, H. (2006). Et ve Et Ürünlerinde Listeria monocytogenes’in İzolasyonu. Van Tıp Dergisi, 13(2), 36–41.
• Bingöl, E. B., Dümen, E., Kahraman, T., Akhan, M., Issa, G., & Ergun, O. (2013). Prevalence of Salmonella spp., Listeria monocytogenes and Escherichia coli O157 in meat and meat products consumed in Istanbul. Medycyna Weterynaryjna-Veterınary Medıcıne-Scıence And Practıce, 69(8), 488–491.
• Bozkurt, B. (2018). Bozkurt, B. (2018). Çiğ Ve Yarı-Pişmiş Bazı Et Ürünlerinde Salmonella Spp. Ve Staphylococcus Aureus’un Belirlenmesi Ve Antibiyotik Dirençliliklerinin Araştırılması. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü, Yüksek Lisans Tezi, Balıkesir. [Yüksek Lisans Tezi]. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü.
• Büyükünal, S. K., Şakar, F. Ş., Turhan, İ., Ergi̇Nbaş, Ç., Sandikçi Altunatmaz, S., Yilmaz Aksu, F., Yilmaz Eker, F., & Kahraman, T. (2015). Geleneksel Türk Fermente Et Ürünlerinde (Sucuk ve Pastırma) Salmonella spp., Listeria monocytogenes, Escherichia coli O157 ve Nitrat-Nitrit Varlığı. Kafkas Universitesi Veteriner Fakultesi Dergisi. https://doi.org/10.9775/kvfd.2015.14238
• Çadırcı, Ö., Gücükoğlu, A., Terzi Güzel, G., Uyanık, T., Abdulahi, A., & Alişarlı, M. (2017). Characterization and Antimicrobial-Resistance Profile of Escherichia coli O157 and O157: H7 Isolated from Modified Atmosphere Packaged Meat Samples. Turkish Journal of Agriculture - Food Science and Technology, 5(10), 1142. https://doi.org/10.24925/turjaf.v5i10.1142-1147.1228
• Çakıcı, N., Demirel Zorba, N. N., & Akçalı, A. (2015). Food industry employees and staphylococcal food poisoning. Turkish Bulletin of Hygiene and Experimental Biology, 72(4), 337–350. https://doi.org/10.5505/TurkHijyen.2015.21704
• Çiftçioğlu, G., & Uğur, M. (1991). Ülkemizde tüketilen beyaz peynirlerde Listeriaların varlığı üzeririne bir araştırma. II. Ulusal Gıda Sempozyumu (Bildiriler), Bursa.
• Dorman, V., Aslan, S., Ceylan, A., Küçük, S. N., Günel, A., Sari, H., Yaşli, N., & Yalim, D. (2010). Aynı fabrikadan yemek alan iki inşaat firması işçilerinde meydana gelen toplu besin zehirlenmesi. Dicle Tıp Dergisi, 37(3), 248–253.
• Dursun, S. (2008). Broiler Piliçlerinden Escherichia coli O157:H7 Serotipinin İdentifikasyonu ve Antibiyotik Duyarlılıklarının Belirlenmesi. [Doktora Tezi]. Adnan Menderes Üniversitesi Sağlık Bilimleri Enstitüsü.
• Eki̇Ci̇, G., Dümen, E., Bayrakal, G. M., & Ergi̇N, S. (2018). Taze Kaşar Peyniri ve Süt Kaymağından İzole Edilen Listeria monocytogenes ve Esherichia coli O157:H7’nin Moleküler Tanımlaması. Kafkas Universitesi Veteriner Fakultesi Dergisi. https://doi.org/10.9775/kvfd.2018.20702
• Elafify, M., Khalifa, H. O., Al-Ashmawy, M., Elsherbini, M., El Latif, A. A., Okanda, T., Matsumoto, T., Koseki, S., & Abdelkhalek, A. (2020). Prevalence and antimicrobial resistance of Shiga toxin-producing Escherichia coli in milk and dairy products in Egypt. Journal of Environmental Science and Health, Part B, 55(3), 265–272. https://doi.org/10.1080/03601234.2019.1686312
• Fantelli, K. (2001). Prevalence and characteristics of Shigatoxin-producing Escherichia coli and Listeria monocytogenes strains isolated from minced meat in Switzerland. International Journal of Food Microbiology, 70(1–2), 63–69. https://doi.org/10.1016/S0168-1605(01)00515-3
• Goldrick, B. (2003). Foodborne Diseases: More efforts needed to meet the Healthy People 2010 objectives. 103 (3): 105–106. The American Journal of Nursing., 103(3), 105–106.
• Gonzalez, A. G. M., Rosa, A. C. P., Andrade, J. R. C., & Tibana, A. (2000). Enteropathogenicity markers in Escherichia coli strains isolated from soft white cheese and poultry in Rio de Janeiro, Brazil. Food Microbiology, 17, 321–328.
• Gülmez, M., & Güven, A. (2001). Beyaz ve çeçil peynirlerinde Campylobacter, Salmonella ve Listeria türlerinin araştırılması. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 7(2), 155–161.
• Hoge, C. W., Gambel, J. M., Srijan, A., Pitarangsi, C., & Echeverria, P. (1998). Trends in Antibiotic Resistance Among Diarrheal Pathogens Isolated in Thailand Over 15 Years. Clinical Infectious Diseases, 26(2), 341–345. https://doi.org/10.1086/516303
• Iannetti, L., Acciari, V. A., Antoci, S., Addante, N., Bardasi, L., Bilei, S., Calistri, P., Cito, F., Cogoni, P., D’Aurelio, R., Decastelli, L., Iannetti, S., Iannitto, G., Marino, A. M. F., Muliari, R., Neri, D., Perilli, M., Pomilio, F., Prencipe, V. A., … Migliorati, G. (2016). Listeria monocytogenes in ready-to-eat foods in Italy: Prevalence of contamination at retail and characterisation of strains from meat products and cheese. Food Control, 68, 55–61. https://doi.org/10.1016/j.foodcont.2016.03.036
• Jantsch, J., Chikkaballi, D., & Hensel, M. (2011). Cellular aspects of immunity to intracellular Salmonella enterica: Cellular microbiology of Salmonella. Immunological Reviews, 240(1), 185–195. https://doi.org/10.1111/j.1600-065X.2010.00981.x
• Jo, M.-Y., Kim, J.-H., Lim, J.-H., Kang, M.-Y., Koh, H.-B., Park, Y.-H., Yoon, D.-Y., Chae, J.-S., Eo, S.-K., & Lee, J. H. (2004). Prevalence and characteristics of Escherichia coli O157 from major food animals in Korea. International Journal of Food Microbiology, 95(1), 41–49. https://doi.org/10.1016/j.ijfoodmicro.2004.01.016
• Kahraman T, & Aydın, A. (2009). Prevalence of Salmonella spp., Escherichia coli O157:H7 and Listeria monocytogenes in meat and meat products in Turkey Prävalenz von Salmonella spp., Escherichia coli O157:H7 und Listeria monocytogenes in Fleisch und Fleischerzeugnissen in der Türkei. Archiv Für Lebensmittelhygiene, Archiv für Lebensmittelhygiene 60: 1, 6-11 (2009), 6–11. https://doi.org/10.2376/0003-925X-60-6
• Kahraman, T., Özmen, G., Özinan, B., & Göksoy, E. O. (2010). Prevalence of Salmonella spp. And Listeria monocytogenes in different cheese types produced in Turkey. BFJ, 112(11), 1230–1236.
• Keerthirathne, T., Ross, K., Fallowfield, H., & Whiley, H. (2016). A Review of Temperature, pH, and Other Factors that Influence the Survival of Salmonella in Mayonnaise and Other Raw Egg Products. Pathogens, 5(4), 63. https://doi.org/10.3390/pathogens5040063
• Lakicevic, B., Nastasijevic, I., & Raseta, M. (2015). Sources of Listeria Monocytogenes Contamination in Retail Establishments. Procedia Food Science, 5, 160–163. https://doi.org/10.1016/j.profoo.2015.09.046
• Madden, R. H., Espie, W. E., Moran, L., McBride, J., & Scates, P. (2001). Occurrence of Escherichia coli O157:H7, Listeria monocytogenes, Salmonella and Campylobacter spp. On beef carcasses in Northern Ireland. Meat Science, 58(4), 343–346. https://doi.org/10.1016/S0309-1740(00)00153-4
• Manguiat, L. S., & Fang, T. J. (2013). Microbiological quality of chicken- and pork-based street-vended foods from Taichung, Taiwan, and Laguna, Philippines. Food Microbiology, 36(1), 57–62. https://doi.org/10.1016/j.fm.2013.04.005
• Maung, A. T., Mohammadi, T. N., Nakashima, S., Liu, P., Masuda, Y., Honjoh, K., & Miyamoto, T. (2019). Antimicrobial resistance profiles of Listeria monocytogenes isolated from chicken meat in Fukuoka, Japan. International Journal of Food Microbiology, 304, 49–57. https://doi.org/10.1016/j.ijfoodmicro.2019.05.016
• Mena, C. (2004). Incidence of Listeria monocytogenes in different food products commercialized in Portugal. Food Microbiology, 21(2), 213–216. https://doi.org/10.1016/S0740-0020(03)00057-1
• Omerovi̇C, M., Müştak, H. K., & Kaya, İ. B. (2017). Escherichia coli Patotiplerinin Virülens Faktörleri. Etlik Veteriner Mikrobiyoloji Dergisi, 28(1), 1–6. https://doi.org/10.35864/evmd.530084
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• Acaröz, U., Gurler, Z., Kara, R., Arslan-Acaröz, D., & Zemheri, F. (2018). Afyonkarahisar İlinde Satışa Sunulan Tavuk Eti ve Sakatatlarında Salmonella spp. Varlığının Belirlenmesi. Kocatepe Veterinary Journal, 1–5. https://doi.org/10.30607/kvj.444137
• Ahmed, A. M., & Shimamoto, T. (2014). Isolation and molecular characterization of Salmonella enterica, Escherichia coli O157:H7 and Shigella spp. From meat and dairy products in Egypt. International Journal of Food Microbiology, 168–169, 57–62. https://doi.org/10.1016/j.ijfoodmicro.2013.10.014
• Akkaya, L., & Alişarlı, M. (2006). Afyonkarahisar’da Tüketime Sunulan Peynirlerde Listeria monocytogenes ve Salmonella spp. Varlığının Belirlenmesi. Yüzüncü Yıl Üniversitesi Veteriner Fakültesi Dergisi, 17(1–2), 87–91.
• Akkaya, L., Alişarlı, M., Kara, R., & Telli, R. (2007). Afyonkarahisar’da Tüketime Sunulan Çig Süt ve Peynirlerde E. coli O157:H7 Varlığının Belirlenmesi. YYÜ VET FAK DERG, 18(1), 1–5.
• Alonso-Hernando, A., Prieto, M., García-Fernández, C., Alonso-Calleja, C., & Capita, R. (2012). Increase over time in the prevalence of multiple antibiotic resistance among isolates of Listeria monocytogenes from poultry in Spain. Food Control, 23(1), 37–41. https://doi.org/10.1016/j.foodcont.2011.06.006
• Arslan, S., & Özdemir, F. (2008). Prevalence and antimicrobial resistance of Listeria spp. In homemade white cheese. Food Control, 19, 360–363.
• Atabey, C. (2011). Piyasada Satışa Sunulan Peynirlerden Elde Edilen Jenerik Escherichia coli Ve Staphylococcus Aureus Suşlarının Antibiyotik Dirençliliklerinin Belirlenerek, Mastitis Kontrol Ve Tedavi Programlarında Kullanılan Antibiyotiklerle İlişkisinin Belirlenmesi. [Yüksek Lisans Tezi]. Adnan Menderes Üniversitesi Sağlık Bilimleri Enstitüsü. Aygun, O., & Pehlivanlar, S. (2006). Listeria spp. In the raw milk and dairy products in Antakya, Turkey. Food Control, 17(8), 676–679. https://doi.org/10.1016/j.foodcont.2005.09.014
• Berktaş, M., Bozkurt, E. N., Bozkurt, H., Alişarlı, M., & Güdücüoğlu, H. (2006). Et ve Et Ürünlerinde Listeria monocytogenes’in İzolasyonu. Van Tıp Dergisi, 13(2), 36–41.
• Bingöl, E. B., Dümen, E., Kahraman, T., Akhan, M., Issa, G., & Ergun, O. (2013). Prevalence of Salmonella spp., Listeria monocytogenes and Escherichia coli O157 in meat and meat products consumed in Istanbul. Medycyna Weterynaryjna-Veterınary Medıcıne-Scıence And Practıce, 69(8), 488–491.
• Bozkurt, B. (2018). Bozkurt, B. (2018). Çiğ Ve Yarı-Pişmiş Bazı Et Ürünlerinde Salmonella Spp. Ve Staphylococcus Aureus’un Belirlenmesi Ve Antibiyotik Dirençliliklerinin Araştırılması. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü, Yüksek Lisans Tezi, Balıkesir. [Yüksek Lisans Tezi]. Balıkesir Üniversitesi Fen Bilimleri Enstitüsü.
• Büyükünal, S. K., Şakar, F. Ş., Turhan, İ., Ergi̇Nbaş, Ç., Sandikçi Altunatmaz, S., Yilmaz Aksu, F., Yilmaz Eker, F., & Kahraman, T. (2015). Geleneksel Türk Fermente Et Ürünlerinde (Sucuk ve Pastırma) Salmonella spp., Listeria monocytogenes, Escherichia coli O157 ve Nitrat-Nitrit Varlığı. Kafkas Universitesi Veteriner Fakultesi Dergisi. https://doi.org/10.9775/kvfd.2015.14238
• Çadırcı, Ö., Gücükoğlu, A., Terzi Güzel, G., Uyanık, T., Abdulahi, A., & Alişarlı, M. (2017). Characterization and Antimicrobial-Resistance Profile of Escherichia coli O157 and O157: H7 Isolated from Modified Atmosphere Packaged Meat Samples. Turkish Journal of Agriculture - Food Science and Technology, 5(10), 1142. https://doi.org/10.24925/turjaf.v5i10.1142-1147.1228
• Çakıcı, N., Demirel Zorba, N. N., & Akçalı, A. (2015). Food industry employees and staphylococcal food poisoning. Turkish Bulletin of Hygiene and Experimental Biology, 72(4), 337–350. https://doi.org/10.5505/TurkHijyen.2015.21704 Çiftçioğlu, G., & Uğur, M. (1991). Ülkemizde tüketilen beyaz peynirlerde Listeriaların varlığı üzeririne bir araştırma. II. Ulusal Gıda Sempozyumu (Bildiriler), Bursa.
• Dorman, V., Aslan, S., Ceylan, A., Küçük, S. N., Günel, A., Sari, H., Yaşli, N., & Yalim, D. (2010). Aynı fabrikadan yemek alan iki inşaat firması işçilerinde meydana gelen toplu besin zehirlenmesi. Dicle Tıp Dergisi, 37(3), 248–253.
• Dursun, S. (2008). Broiler Piliçlerinden Escherichia coli O157:H7 Serotipinin İdentifikasyonu ve Antibiyotik Duyarlılıklarının Belirlenmesi. [Doktora Tezi]. Adnan Menderes Üniversitesi Sağlık Bilimleri Enstitüsü.
• Eki̇Ci̇, G., Dümen, E., Bayrakal, G. M., & Ergi̇N, S. (2018). Taze Kaşar Peyniri ve Süt Kaymağından İzole Edilen Listeria monocytogenes ve Esherichia coli O157:H7’nin Moleküler Tanımlaması. Kafkas Universitesi Veteriner Fakultesi Dergisi. https://doi.org/10.9775/kvfd.2018.20702
• Elafify, M., Khalifa, H. O., Al-Ashmawy, M., Elsherbini, M., El Latif, A. A., Okanda, T., Matsumoto, T., Koseki, S., & Abdelkhalek, A. (2020). Prevalence and antimicrobial resistance of Shiga toxin-producing Escherichia coli in milk and dairy products in Egypt. Journal of Environmental Science and Health, Part B, 55(3), 265–272. https://doi.org/10.1080/03601234.2019.1686312
• Fantelli, K. (2001). Prevalence and characteristics of Shigatoxin-producing Escherichia coli and Listeria monocytogenes strains isolated from minced meat in Switzerland. International Journal of Food Microbiology, 70(1–2), 63–69. https://doi.org/10.1016/S0168-1605(01)00515-3
• Goldrick, B. (2003). Foodborne Diseases: More efforts needed to meet the Healthy People 2010 objectives. 103 (3): 105–106. The American Journal of Nursing., 103(3), 105–106.
• Gonzalez, A. G. M., Rosa, A. C. P., Andrade, J. R. C., & Tibana, A. (2000). Enteropathogenicity markers in Escherichia coli strains isolated from soft white cheese and poultry in Rio de Janeiro, Brazil. Food Microbiology, 17, 321–328.
• Gülmez, M., & Güven, A. (2001). Beyaz ve çeçil peynirlerinde Campylobacter, Salmonella ve Listeria türlerinin araştırılması. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 7(2), 155–161.
• Hoge, C. W., Gambel, J. M., Srijan, A., Pitarangsi, C., & Echeverria, P. (1998). Trends in Antibiotic Resistance Among Diarrheal Pathogens Isolated in Thailand Over 15 Years. Clinical Infectious Diseases, 26(2), 341–345. https://doi.org/10.1086/516303
• Iannetti, L., Acciari, V. A., Antoci, S., Addante, N., Bardasi, L., Bilei, S., Calistri, P., Cito, F., Cogoni, P., D’Aurelio, R., Decastelli, L., Iannetti, S., Iannitto, G., Marino, A. M. F., Muliari, R., Neri, D., Perilli, M., Pomilio, F., Prencipe, V. A., … Migliorati, G. (2016). Listeria monocytogenes in ready-to-eat foods in Italy: Prevalence of contamination at retail and characterisation of strains from meat products and cheese. Food Control, 68, 55–61. https://doi.org/10.1016/j.foodcont.2016.03.036
• Jantsch, J., Chikkaballi, D., & Hensel, M. (2011). Cellular aspects of immunity to intracellular Salmonella enterica: Cellular microbiology of Salmonella. Immunological Reviews, 240(1), 185–195. https://doi.org/10.1111/j.1600-065X.2010.00981.x
• Jo, M.-Y., Kim, J.-H., Lim, J.-H., Kang, M.-Y., Koh, H.-B., Park, Y.-H., Yoon, D.-Y., Chae, J.-S., Eo, S.-K., & Lee, J. H. (2004). Prevalence and characteristics of Escherichia coli O157 from major food animals in Korea. International Journal of Food Microbiology, 95(1), 41–49. https://doi.org/10.1016/j.ijfoodmicro.2004.01.016
• Kahraman T, & Aydın, A. (2009). Prevalence of Salmonella spp., Escherichia coli O157:H7 and Listeria monocytogenes in meat and meat products in Turkey Prävalenz von Salmonella spp., Escherichia coli O157:H7 und Listeria monocytogenes in Fleisch und Fleischerzeugnissen in der Türkei. Archiv Für Lebensmittelhygiene, Archiv für Lebensmittelhygiene 60: 1, 6-11 (2009), 6–11. https://doi.org/10.2376/0003-925X-60-6
• Kahraman, T., Özmen, G., Özinan, B., & Göksoy, E. O. (2010). Prevalence of Salmonella spp. And Listeria monocytogenes in different cheese types produced in Turkey. BFJ, 112(11), 1230–1236.
• Keerthirathne, T., Ross, K., Fallowfield, H., & Whiley, H. (2016). A Review of Temperature, pH, and Other Factors that Influence the Survival of Salmonella in Mayonnaise and Other Raw Egg Products. Pathogens, 5(4), 63. https://doi.org/10.3390/pathogens5040063
• Lakicevic, B., Nastasijevic, I., & Raseta, M. (2015). Sources of Listeria Monocytogenes Contamination in Retail Establishments. Procedia Food Science, 5, 160–163. https://doi.org/10.1016/j.profoo.2015.09.046
• Madden, R. H., Espie, W. E., Moran, L., McBride, J., & Scates, P. (2001). Occurrence of Escherichia coli O157:H7, Listeria monocytogenes, Salmonella and Campylobacter spp. On beef carcasses in Northern Ireland. Meat Science, 58(4), 343–346. https://doi.org/10.1016/S0309-1740(00)00153-4
• Manguiat, L. S., & Fang, T. J. (2013). Microbiological quality of chicken- and pork-based street-vended foods from Taichung, Taiwan, and Laguna, Philippines. Food Microbiology, 36(1), 57–62. https://doi.org/10.1016/j.fm.2013.04.005
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