The Determination of Presence of Listeria monocytogenes in Ground Meat Sold in Istanbul

Year 2023, , 53 - 66, 01.03.2023

Arda Alara Uludağ , Elif Özlem Arslan Aydoğdu , Ayten Kimiran

https://doi.org/10.35378/gujs.972909

Cited By: 1

Abstract

Listeria monocytogenes that the most common human listeriosis agent is one of 21 species of the Listeria genera. In fact, the mortality rate of listeriosis is higher than that of the more common foodborne pathogens such as Vibrio species or Salmonella Enteritidis. This study was aimed to determine the L. monocytogenes contamination in different minced meat samples. In this study, 100 minced meat samples purchased from different butchers in 11 districts of Istanbul between December 2018 and November 2019 were examined for the presence of L. monocytogenes. Isolates were molecularly confirmed for the presence of the iap and hlyA gene regions. It was determined that 21 biochemically defined isolates were susceptible to tetracycline and ampicillin, while resistant to amoxicillin/clavulanic acid, penicillin, cefaclor, and vancomycin. In addition, it was determined that only 16 of these 21 isolates were L. monocytogenes in terms of iap and hlyA gene regions. L. monocytogenes incidence in minced meat sold in Istanbul is low (17%), we believe that these contamination rates indicate a significant risk to public health due to cross-contamination and raw consumption of minced meat.

Keywords

Listeria monocytogenes, Minced meat, hlyA 16S rRNA, Antibiotic susceptibility

Project Number

FYL-2018-31547

References

• [1] Junttila, J.R., Niemelä, S.I., and Hirn, J., “Minimum growth temperatures of Listeria monocytogenes and non-haemolytic Listeria”, Journal of Applied Bacteriology, 65(4): 321-327, (1988).
• [2] Walker, S.J., and Stringer, M.F., “Growth of Listeria monocytogenes and Aeromonas hydrophila at chill temperatures”, Campden food preservation research association technical memorandum no.462, Campden Food Preservation Research Association, Chipping Campden, United Kingdom, 20-23, (1987).
• [3] Lovett, J., “Listeria monocytogenes”, In: Doyle, M.P., (ed.), Marcel Dekker, New York, USA, 283-310, (1989).
• [4] Liu, D., “Handbook of Listeria monocytogenes”, CRC press, Boca Raton, USA, 24-34, (2008).
• [5] Sleator, R.D., Gahan, C.G.M., and Hill, C., “A postgenomic appraisal of osmotolerance in Listeria monocytogenes”, Applied and Environmental Microbiology, 69(1): 1-9, (2003).
• [6] Liu, D., Lawrence, M.L., Ainsworth, A.J., and Austin, F.W., “Comparative assessment of acid, alkali and salt tolerance in Listeria monocytogenes virulent and avirulent strains”, Federation of European Microbiological Societies Microbiology Letters, 243(2): 373-378, (2005).
• [7] Goulet, V., Jacquet, C., Martin, P., Vaillant, V., Laurent, E., and de Valk, H., “Surveillance of human listeriosis in France, 2001-2003”, Eurosurveillance, 11(6): 3-4, (2006).
• [8] Farber, J.M., and Peterkin, P.I., “Listeria monocytogenes, a food-borne pathogen”, Microbiology and Molecular Biology Reviews, 55(3): 476-511, (1991).
• [9] Lorber, B., “Listeriosis”, Clinical Infectious Diseases, 24(1): 1-11, (1997).
• [10] Vazquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J., and Kreft, J., “Listeria pathogenesis and molecular virulence determinants”, Clinical Microbiology Reviews, 14(3): 584-640, (2001).
• [11] Altekruse, S.F., Cohen, M.L., and Swerdlow, D.L., “Emerging foodborne diseases”, Emerging Infectious Diseases, 3(3): 285-293, (1997).
• [12] Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M., and Tauxe, R.V., “Food-related illness and death in the United States”, Emerging Infectious Diseases, 5(5): 607-625, (1999).
• [13] Nyfeldt, A., “Etiologie de la mononucleose infecteuse”, Comptes Rendus des Seances de la Societe de Biologie, 101: 590-591, (1929).
• [14] Schlech, W.F., Lavigne, P.M., Bortolussi, R.A., Allen, A.C., Haldane, E.V., Wort, A.J., Hightower, A.W., Johnson, S.E., King, S.H., Nicholls, E.S., and Broome, C.V., “Epidemic listeriosis-evidence for transmission by Food”, New England Journal of Medicine, 308(4): 203-206, (1983).
• [15] Fleming, D.W., Cochi, S.L., MacDonald, K.L., Brondum, J., Hayes, P.S., Plikaytis, B.D., Holmes, M.B., Audurier, A., Broome, C.V., and Reingold, A.L., “Pasteurized milk as a vehicle of infection in an outbreak of listeriosis”, New England Journal of Medicine, 312(7): 404-407, (1985).
• [16] Ho, J.L., “An outbreak of type 4b Listeria monocytogenes infection involving patients from eight Boston hospitals”, Archives of Internal Medicine, 146(3): 520-524, (1986).
• [17] McLauchlin, J., Hall, S.M., Velani, S.K., and Gilbert, R.J., “Human listeriosis and pate: a possible association”, British Medical Journal, 303(6805): 773-775, (1991).
• [18] Linnan, M.J., Mascola, L., Lou, X.D., Goulet, V., May, S., Salminen, C., Hird, D.W., Yonekura, M.L., Hayes, P., Weaver, R., Audurier, A., Plikaytis, B.D., Fannin, S.L., Kleks, A., and Broome, C.V., “Epidemic listeriosis associated with Mexican-style cheese”, New England Journal of Medicine, 319(13): 823-828, (1988).
• [19] Riedo, F.X., Pinner, R.W., Tosca, M.D.L., Cartter, M.L., Graves, L.M., Reeves, M.W., Weaver, R.E., Plikaytis, B.D., and Broome, C., “A point-source foodborne listeriosis outbreak: documented incubation period and possible mild illness”, Journal of Infectious Diseases, 170(3): 693-696, (1994).
• [20] Goulet, V., Jacquet, C., Vaillant, V., Rebière, I., Mouret, E., Lorente, C., Maillot, E., Staïner, F., and Rocourt, J., “Listeriosis from consumption of raw-milk cheese”, The Lancet, 345(8964): 1581-1582, (1995).
• [21] Schwartz, B., Broome, C., Brown, G., Hightower, A., Ciesielski, C., Gaventa, S., Gellin, B., Mascola, L., and Listeriosis Study Group, “Association of sporadic listeriosis with consumption of uncooked hot dogs and undercooked chicken”, The Lancet, 332(8614): 779-782, (1988).
• [22] Schuchat, A., “Role of foods in sporadic listeriosis”, Journal of the American Medical Association, 267(15): 2041, (1992).
• [23] Nguyen, M.H., and Yu, V.L., “Listeria monocytogenes peritonitis in cirrhotic patients”, Digestive Diseases and Sciences, 39(1): 215-218, (1994).
• [24] Soyutemiz, E., “Et ve et ürünlerinde mikrobiyal bozulmalar”, The Journal of Food, 3: 52-57, (2000).
• [25] Evans, M.R., Swaminathan, B., Graves, L.M., Altermann, E., Klaenhammer, T.R., Fink, R.C., Kernodle, S., and Kathariou, S., “Genetic markers unique to Listeria monocytogenes serotype 4b differentiate epidemic clone II (hot dog outbreak strains) from other lineages”, Applied and Environmental Microbiology, 70(4): 2383-2390, (2004).
• [26] Mead, P.S., Dunne, E.F., Graves, L., Wiedmann, M., Patrick, M., Hunter, S., Salehi, E., Mostashari, F., Craig, A., Mshar, P., Bannerman, T., Sauders, B.D., Hayes, P., Dewitt, W., Sparling, P., Griffin, P., Morse, D., Slutsker, L., and Swaminathan, B., “Nationwide outbreak of listeriosis due to contaminated meat”, Epidemiology and Infection, 134(4): 744-751, (2005).
• [27] Dempster, J.F., “A note on the hygiene of meat mincing machines”, Epidemiology and Infection, 71(4): 739-744, (1973).
• [28] Pivnick, H., Erdman, I.E., Collins-Thompsonn, D., Roberts, G., Johhnston, M.A., Conley, D.R., Lachapelle, G., Purvis, U.T., Foster, R., and Milling, M., “Proposed microbiological standards for ground beef based on a Canadian survey”, Journal of Milk and Food Technology, 39(6): 408-412, (1976).
• [29] Tekinsen, O.C., Yurtyeri, A., and Mutluer, B., “Ankara'da satılan hazır kıymaların bakteriyolojik kalitesi”, Veterinary Journal of Ankara University, 1(2): 45-63, (1980).
• [30] Akilli, A., “Ankara’da süper marketlerde satılan hazır kıymaların mikrobiyolojik ve kimyasal kaliteleri ile tek tırnaklı hayvan etleri yönünden incelenmesi üzerine araştırmalar”, Journal of Etlik Veterinary Microbiology, 5: 4-5, (1982).
• [31] Sancak, Y.C., Boynukara B., and Agaoglu S., “Van'da tüketime sunulan kıymaların mikrobiyolojik kalitesi”, The Journal of the Faculty of Veterinary Medicine University of Yuzuncu Yil, 4(1): 73-86, (1993).
• [32] Guven, A., Gulmez, M., and Kamber, U., “Kars ilinde tüketime sunulan kıymalarda bazı patojen mikroorganizmaların araştırılması ve kıymaların mikrobiyolojik kalitesinin belirlenmesi”, Journal of the Faculty of Veterinary Medicine, Kafkas University, 3(1): 57-65, (1997).
• [33] Gonulalan, Z., and Kose, A., “Kayseri ilinde satışa sunulan sığır kıymalarının mikrobiyolojik kalitesi”, Fırat University Medical Journal of Health Sciences, 17(1): 49-53, (2003).
• [34] Siriken, B., “The presence of Yersinia enterocolitica and other Yersinia species in ground beef in Aydın”, Turkey, Turkish Journal of Veterinary and Animal Sciences, 28(3): 489-495, (2004).
• [35] Doyle, M.P., Loneragan, G.H., Scott, H.M., and Singer, R.S., “Antimicrobial resistance: challenges and perspectives”, Comprehensive Reviews in Food Science and Food Safety, 12(2): 234-248, (2013).
• [36] Jones, E.M., and MacGowan, A.P., “Antimicrobial chemotherapy of human infection due to Listeria monocytogenes”, European Journal of Clinical Microbiology and Infectious Diseases, 14(3): 165-175, (1995).
• [37] Walsh, D., Duffy, G., Sheridan, J.J., Blair, I.S., and McDowell, D.A., “Antibiotic resistance among Listeria, including Listeria monocytogenes in retail foods”, Journal of Applied Microbiology, 90(4): 517-522, (2001).
• [38] MacGowan, A.P., Holt, H.A., and Reeves, D.S., “In-vitro synergy testing of nine antimicrobial combinations against Listeria monocytogenes”, Journal of Antimicrobial Chemotherapy, 25(4): 561-566, (1990).
• [39] Hof, H., “Therapeutic activities of antibiotics in listeriosis”, Infection, 19(4): 229-233, (1991).
• [40] Liu, D., “Handbook of Listeria monocytogenes”, CRC Press, Boca Raton, USA, 31, (2008).
• [41] Mcclain, D., and Lee, W.H., “Development of USDA-FSIS method for isolation of Listeria monocytogenes from raw meat and poultry”, Journal of Association of Official Analytical Collaboration International, 71(3): 660-664, (1988).
• [42] Kohler, S., Leimeister-Wachter, M., Chakrabotry, T., Lottspeich, F., and Goebel, W., “The gene coding for protein p60 of Listeria monocytogenes and its use as a specific probe for Listeria monocytogenes”, Infection and Immunity, 58(6): 1943-1950, (1990).
• [43] Bohnert, M., Dilasser, F., Dalet, C., Mengaud, J., and Cossart, P., “Use of specific oligonucleotides for direct enumeration of Listeria monocytogenes in food samples by colony hybridization and rapid detection by PCR”, Research in Microbiology, 143(3): 271-280, (1992).
• [44] Lane, D.J., “16S/23S rRNA sequencing, Nucleic acid techniques in bacterial systematics”, In: Stackebrandt, E., Goodfellow, M. (eds.), John Wiley and Sons, New York, 115-175, (1991).
• [45] National Committee for Clinical Laboratory Standards (NCCLS), “Performance standards for antimicrobial disk susceptibility tests: approved standard, M31-A3”, Wayna, PA, USA, (2010).
• [46] Ray, B., “Fundamental Food Microbiology”, 3rd ed., CRC press, Boca Raton, USA, 367-370, (2003).
• [47] Vlaemynck, G., Lafarge, V., and Scotter, S., “Improvement of the detection of Listeria monocytogenes by the application of ALOA, a diagnostic, chromogenic isolation medium”, Journal of Applied Microbiology, 88(3): 430-441, (2000).
• [48] Guven, A., and Patir, B., “Elazığ ilinde tüketime sunulan et ve bazı et ürünlerinde Listeria türlerinin araştırılması”, Turkish Journal of Veterinary and Animal Sciences, 22:205-212, (1998).
• [49] Berktas, M., Bozkurt, E.N., Bozkurt, H., Alisarli, M., and Guducuoglu, H., “Et ve et ürünlerinden Listeria monocytogenes’in izolasyonu”, Van Medical Journal, 13(2): 36-41, (2006).
• [50] Akpolat, N.O., Elci, S., Atmaca, S., and Gul, K., “Listeria monocytogenes in products of animal origin in Turkey”, Veterinary Research Communications, 28(7): 561-567, (2004).
• [51] Heredia, N., García, S., Rojas, G., and Salazar, L., “Microbiological condition of ground meat retailed in Monterrey, Mexico”, Journal of Food Protection, 64(8): 1249-1251, (2001).
• [52] De Simón, M., Tarragó, C., and Ferrer, M.D., “Incidence of Listeria monocytogenes in fresh foods in Barcelona (Spain)”, International Journal of Food Microbiology, 16(2): 153-156, (1992).
• [53] Wang, X.M., Lu, X.F., Yin, L., Liu, H.F., Zhang, W.J., Si, W., Yu, S.Y., Shao, M.L., and Liu, S.G., “Occurrence and antimicrobial susceptibility of Listeria monocytogenes isolates from retail raw foods”, Food Control, 32(1): 153-158, (2013).
• [54] Sireli U.T., “Hazır kıymalarda Listeria türlerinin araştırılması”, (Ph.D), Ankara University Graduate School of Health Sciences, Ankara, 32-34, (1996).
• [55] Aydemir Atasever, M., and Atasever, M., “Kıymalarda bazı patojenlerin izolasyon ve identifikasyonu”, Acta Veterinaria Eurasia, 41(1): 60-68, (2015).
• [56] Ciftcioglu, G., “Kıyma, sucuk ve tavuk etlerinde L. monocytogenes’in mevcudiyeti üzerine araştırmalar”, (Ph.D), Istanbul University Graduate School of Health Sciences, Istanbul, 51, (1992).
• [57] Sireli, U.T., and Erol, I., “Hazır kıymalarda Listeria türlerinin araştırılması”, Turkish Journal of Veterinary and Animal Sciences, 23: 373-380, (1999).
• [58] Truscott, R.B., and Mcnab, W.B., “Comparison of media and procedures for the isolation of Listeria monocytogenes from ground beef”, Journal of Food Protection, 51(8): 626-628, (1988).
• [59] Farber, J.M., Sanders, G.W., and Johnston, M.A., “A survey of various foods for the presence of Listeria species”, Journal of Food Protection, 52(7): 456-458, (1989).
• [60] Ryu, C.H., Igimi, S., Inoue, S., and Kumagai, S., “The incidence of Listeria species in retail foods in Japan”, International Journal of Food Microbiology, 16(2): 157-160, (1992).
• [61] Fenlon, D.R., Wilson, J., and Donachie, W., “The incidence and level of Listeria monocytogenes contamination of food sources at primary production and initial processing”, Journal of Applied Bacteriology, 81(6): 641-650, (1996).
• [62] Al-Nabulsi, A.A., Osaili, T.M., Awad, A.A., Olaimat, A.N., Shaker, R.R., and Holley, R.A., “Occurrence and antibiotic susceptibility of Listeria monocytogenes isolated from raw and processed meat products in Amman, Jordan”, Ciencia y Technogia Alimentaria-Journal of Food, 13(3): 346-352, (2015).
• [63] Gómez, D., Iguácel, L., Rota, M., Carramiñana, J., Ariño, A., and Yanguela, J., “Occurrence of Listeria monocytogenes in ready-to-eat meat products and meat processing plants in Spain”, Foods, 4(4): 271-282, (2015).
• [64] Roberts, D., “Sources of infection: food”, The Lancet, 336(8719): 859-861, (1990).
• [65] Skovgaard, N., and Morgen, C.A., “Detection of Listeria spp. in faeces from animals, in feeds, and in raw foods of animal origin”, International Journal of Food Microbiology, 6(3): 229-242, (1988).
• [66] Abay, S., Irkin, R., Aydin, F., Mustak, H.K., and Diker, K.S., “The prevalence of major foodborne pathogens in ready-to-eat chicken meat samples sold in retail markets in Turkey and the molecular characterization of the recovered isolates”, Food Science and Technology, 81: 202-209, (2017).
• [67] Yang, D., Wu, X., Yu, X., He, L., Shah, N.P., and Xu, F., “Mutual growth-promoting effect between Bifidobacterium bifidum WBBI03 and Listeria monocytogenes CMCC 54001”, Journal of Dairy Science, 100(5): 3448-3462, (2017).
• [68] Suo, B., He, Y., Tu, S.I., and Shi, X., “A multiplex real-time polymerase chain reaction for simultaneous detection of Salmonella spp., Escherichia coli O157, and Listeria monocytogenes in meat products”, Foodborne Pathogens and Disease, 7(6): 619-628, (2010).
• [69] Sanlibaba, P., Tezel, B.U., Cakmak, G.A., Keski̇n, R., and Akceli̇k, M., “Occurrence of Listeria spp. and antibiotic resistance profiles of Listeria monocytogenes from raw meat products in Turkey”, Italian Journal of Food Science, 32(1): 234-250, (2020).
• [70] Aarestrup, F.M., and Wegener, H.C., “The effects of antibiotic usage in food animals on the development of antimicrobial resistance of importance for humans in Campylobacter and Escherichia coli”, Microbes and Infection, 1(8): 639-644, (1999).
• [71] http://www.akilciilac.gov.tr/?page_id=826. Access date: 06.07.2021.
• [72] Olsen, S.J., DeBess, E.E., McGivern, T.E., Marano, N., Eby, T., Mauvais, S., Balan, V.K., Zirnstein, G., Cieslak, P.R., and Angulo, F.J., “A nosocomial outbreak of fluoroquinolone-resistant Salmonella infection”, New England Journal of Medicine, 344(21): 1572-1579, (2001).
• [73] Smith, D.L., Harris, A.D., Johnson, J.A., Silbergeld, E.K., and Morris, J.G., “Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria”, Proceedings of the National Academy of Sciences, 99(9): 6434-6439, (2002).
• [74] Courvalin, P., “Transfer of antibiotic resistance genes between gram-positive and gram-negative bacteria”, Antimicrobial Agents and Chemotherapy, 38(7): 1447-1451, (1994).
• [75] Poyart-Salmeron, C., Carlier, C., Trieu-Cuot, P., Courvalin, P., and Courtieu, A.L., “Transferable plasmid-mediated antibiotic resistance in Listeria monocytogenes”, The Lancet, 335(8703): 1422-1426, (1990).
• [76] Slade, P.J., and Collins-Thompson, D.L., “Listeria, plasmids, antibiotic resistance, and food”, The Lancet, 336: 1004, (1990).
• [77] Facinelli, B., Giovanetti, E., Varaldo, P.E., Casolar I.P., and Fabio, U., “Antibiotic resistance in foodborne Listeria”, The Lancet, 338(8777): 1272, (1991).
• [78] Hadorn, K., Hächler, H., Schaffner, A., and Kayser, F.H., “Genetic characterization of plasmid-encoded multiple antibiotic resistance in a strain of Listeria monocytogenes causing endocarditis”, European Journal of Clinical Microbiology and Infectious Diseases, 12(12): 928-937, (1993).
• [79] Charpentier, E., Gerbaud, G., Jacquet, C., Rocourt, J., and Courvalin, P., “Incidence of antibiotic resistance in Listeria species”, The Journal of Infectious Diseases, 172(1): 277-281, (1995).
• [80] Roberts, M.C., Facinelli, B., Giovanetti, E., and Varaldo, P.E., “Transferable erythromycin resistance in Listeria spp. isolated from food”, Applied and Environmental Microbiology, 62(1): 269-270, (1996).
• [81] Charpentier, E., and Courvalin, P., “Antibiotic resistance in Listeria spp.”, Antimicrobial Agents and Chemotherapy, 43(9): 2103-2108, (1999).
• [82] Yucel, N., Citak, S., and Onder, M., “Prevalence and antibiotic resistance of Listeria species in meat products in Ankara, Turkey”, Food Microbiology, 22(2-3): 241-245, (2005).
• [83] Gómez, D., Azón, E., Marco, N., Carramiñana, J.J., Rota, C., Ariño, A., and Yanguela, J., “Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment”, Food Microbiology, 4: 61-65, (2014).
• [84] Camargo, A.C., de Castilho, N.P.A., da Silva, D.A.L., Vallim, D.C., Hofer, E., and Nero, L.A., “Antibiotic resistance of Listeria monocytogenes isolated from meat-processing environments, beef products, and clinical cases in Brazil”, Microbial Drug Resistance, 21(4): 458-462, (2015).
• [85] Dogruer, Y., Telli, N., Telli, A.E., and Guner, A., “Presence and antibiotic susceptibility of Listeria monocytogenes in retail meat and meat products”, International Journal of Biological Research, 3(2): 76-81, (2015).
• [86] Ennaji, H., Timinouni, M., Ennaji, M.M., Hassar, M., and Cohen, N., “Characterization and antibiotic susceptibility of Listeria monocytogenes isolated from poultry and red meat in Morocco”, Infection and Drug Resistance, 1: 45-50, (2008).
• [87] Khen, B.K., Lynch, O.A., Carroll, J., McDowell, D.A., and Duffy, G., “Occurrence, antibiotic resistance and molecular characterization of Listeria monocytogenes in the beef chain in the republic of Ireland”, Zoonoses and Public Health, 62(1): 11-17, (2015).