Nil KAYA, Elif Özlem ARSLAN AYDOĞDU, Ayten KİMİRAN

Isolation and Identification of Listeria spp. from White Cheese Samples Presented for Consumption in Istanbul

In this study, 119 feta cheese samples taken from different vendors in Istanbul were examined for the presence of L. monocytogenes. Isolates were confirmed by PCR method using iap and hlyA primers, and the antibiotic susceptibility of the identified strains was performed by the Kirby-Bauer protocol. Seven Listeria spp. was isolated from three (% 2.52) of 119 cheese samples analyzed. The seven Listeria spp. obtained from these three samples were found to contain the iap gene region but not the hlyA gene region. As a result of the sequence analysis using the 16S rRNA gene region, it was determined that these isolates were L. seeligeri. As a result of antibiotic susceptibility tests, it was observed that L. seeligeri isolates were showed ciprofloxacin (% 85.71) and penicillin (% 42.85) resistance. All strains were susceptible to amikacin, amoxicillin/clavulanic acid, chloramphenicol, rifampin, gentamicin, cefaclor, ampicillin, trimethoprim-sulfamethoxazole, tetracycline, vancomycin, and clarithromycin antibiotics. The detection of Listeria bacteria in feta cheese samples made with pasteurized milk revealed that packaging, distribution, and storage practices following the pasteurization process should be followed more strictly. It is recommended to apply controls at each stage to prevent contamination.

Keywords:

L. monocytogenes, Feta cheese iap, hlyA, Antibiotic sensitivity,

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[1] J. R. Junttila, S. Niemelä, and J. Hirn, “Minimum growth temperatures of Listeria monocytogenes and non‐haemolytic Listeria,” Journal of Applied Bacteriology, vol. 65, no. 4, pp. 321–327, 1988.
[2] M. E. Parish and D. P. Higgins, “Survival of Listeria monocytogenes in low pH model broth systems,” Journal of Food Protection, vol. 52, no. 3, pp. 144–147, 1989.
[3] S. Galsworthy, S. Girdler and S. Koval, “Chemotaxis in Listeria monocytogenes,” Acta Microbiologica Hungarica, vol. 37, no. 1, pp. 81–85, 1990.
[4] S. M. George and B. M. Lund, “The effect of culture medium and aeration on growth of Listeria monocytogenes at pH 4.5,” Letters in Applied Microbiology, vol. 15, no. 2, pp. 49–52, 1992.
[5] J. M. Farber and C. Addison, “RAPD typing for distinguishing species and strains in the genus Listeria,” Journal of Applied Bacteriology, vol. 77 no. 3, pp. 242–250, 1994.
[6] J. Farber and P. Peterkin, “Listeria monocytogenes, a food-borne pathogen,” Microbiology and Molecular Biology Reviews, vol. 55, no. 3, pp. 476–511, 1991.
[7] A. Schuchat, B. Swaminathan and C. V. Broome, “Epidemiology of human listeriosis,” Clinical microbiology reviews, vol. 4, no. 2, pp. 169–183, 1991.
[8] R. W. Pinner et al., “Role of Foods in Sporadic Listeriosis: II. Microbiologic and Epidemiologic Investigation,” Jama, vol. 267, no. 15, pp. 2046–2050, 1992.
[9] J. Rocourt and P. Cossart, “Listeria monocytogenes,” in Food Microbiology Fundamentals and Frontiers, M. P. Doyle, L. R. Beuchat, T. J. Montville, Eds., Washington, DC, USA: ASM, 1997, pp. 237–352.
[10] B. Gudbjörnsdottir et al., “The incidence of Listeria monocytogenes in meat, poultry and seafood plants in the Nordic countries,” Food Microbiology, vol. 21, no. 2, pp. 217–225, 2004.
[11] P. S. Mead et al., “Food-related illness and death in the United States,” Emerging Infectious Diseases, vol. 5, no. 5, pp. 607, 1999.
[12] P. S. Mead et al., “Nationwide outbreak of listeriosis due to contaminated meat,” Epidemiology & Infection, vol. 134, no. 4, pp. 744–751, 2006.
[13] E. Jones and A. MacGowan, “Antimicrobial chemotherapy of human infection due to Listeria monocytogenes,ˮ European Journal of Clinical Microbiology and Infectious Diseases, vol. 14, no. 3, pp. 165–175, 1995.
[14] P. Kaynar, “Ülkemiz Peynirleri Üzerine Mikrobiyolojik Araştırmalar,ˮ Türk Mikrobiyoloji Cemiyeti Dergisi, vol. 41, no. 1, pp. 1–8, 2011.
[15] FDA, “Listeria isolation; revised method of analysis: notice, Bacteriological analytical manual,ˮ Chapter 29, U.S. Food and Drug Administration, pp. 44147-44153, 1988.
[16] A. D. Hitchins, “Listeria monocytogenes,ˮ in Bacteriological Analytical Manual Revision A, G. J. Jackson, Ed., Gaithersburg, MD, USA: AOAC International, 1995, pp. 1001–1013.
[17] NCCLS–National Committee for Clinical Laboratory Standards, Performance Standards for Antimicrobial Disk Susceptibility Tests, Approved Standard, M2-A6, NCCLS Publications, Wayne, PA, USA, 1997.
[18] S. Köhler, M. Leimeister-Wächter, T. Chakraborty, F. Lottspeich and W. Goebel, “The gene coding for protein p60 of Listeria monocytogenes and its use as a specific probe for Listeria monocytogenes,ˮ Infection and Immunity, vol. 58, no. 6, pp. 1943–1950, 1990.
[19] M. Bohnert, F. Dilasser, C. Dalet, J. Mengaud and P. Cossart, “Use of specific oligonucleotides for direct enumeration of Listeria monocytogenes in food samples by colony hybridization and rapid detection by PCR,ˮ Research in Microbiology, vol. 143, no. 3, pp. 271–280, 1992.
[20] S. Elmas, “Aydın ilindeki semt pazarlarında satışa sunulan beyaz, tulum ve lor peynirlerinde Listeria monocytogenes ve Salmonella spp. varlığının araştırılması,ˮ M.S. thesis, Dept. Food Hygiene and Technol., Adnan Menderes Univ., Aydın, Turkey, 2014.
[21] M. Gülmez, A. Güven, and A. Çetinkaya, “Kars'ta tüketime sunulan taze ve salamura beyaz peynirlerin bazı mikrobiyolojik ve kimyasal özellikleri,ˮ Kafkas Üniversitesi Veteriner Fakültesi Dergisi, vol. 7, no. 1, pp. 55–62, 2001.
[22] Z. Kaynar, P. Kaynar and C. Koçak, Ankara piyasasında tüketime sunulan beyaz peynirlerin hijyenik kalitelerinin belirlenmesi üzerine bir araştırma. Türk Hijyen ve Deneysel Biyoloji Dergisi, vol. 62, no. 1, pp. 1–10, 2005.
[23] Z. T. Alas, “Ankara piyasasında tüketime sunulan beyaz peynir ve sade dondurmada Listeria monocytogenes, Bacillus cereus, fekal koliform ve E. coli varlığı,ˮ M.S. thesis, Dept. Biol., Gazi Univ., Ankara, Turkey, 2004.
[24] B. Çetin, S. Karasu, A. Atik and M. Z. Durak, “Investigation of Microbiological Quality of Some Dairy Products in Kirklareli: Detection of Salmonella spp. and Listeria monoctyogenes by Real Time PCR,,ˮ Journal of Tekirdag Agricultural Faculty, vol. 12, no. 1, pp. 74–80, 2015.
[25] E. Atil, H. Ertas and G. Ozbey, “Isolation and molecular characterization of Listeria spp. from animals, food and environmental samples,ˮ Veterinarni Medicina, vol. 56, no. 8, pp. 386–394, 2011.
[26] E. Rahimi, M. Ameri and H. Momtaz, “Prevalence and antimicrobial resistance of Listeria species isolated from milk and dairy products in Iran,ˮ Food Control, vol. 21, no. 11, pp. 1448–1452, 2010.
[27] L. Akkaya and M. Alişarlı, “Afyonkarahisar'da tüketime sunulan peynirlerde Listeria monocytogenes ve Salmonella spp. varlığının belirlenmesi,ˮ Yüzüncü Yıl Üniversitesi Veteriner Fakültesi Dergisi, vol. 17, no. 1, pp. 87–91, 2006.
[28] O. Aygun and S. Pehlivanlar, “Listeria spp. in the raw milk and dairy products in Antakya, Turkey,ˮ Food Control, vol. 17, no. 8, 676–679, 2006.
[29] Z. G. Ceylan and A. K. Demirkaya, “Erzurum piyasasından temin edilen salamura beyaz peynirlerde Listeria monocytogenes varlığı ve bazı mikrobiyolojik özeliklerinin belirlenmesi,ˮ Atatürk Üniversitesi Ziraat Fakültesi Dergisi, vol. 38, no. 2, 137–141, 2007.
[30] S. H. Elshinaway, A. M. Meshref, M. M. Zeinhom and D. A. Hafez, “Incidence of Listeria species in some dairy products Inbeni-Suef Governorate,ˮ Assiut Veterinary Medical Journal, vol. 63, no. 152, pp. 5–13, 2017.
[31] S. Arslan and F. Özdemir, “Prevalence and antimicrobial resistance of Listeria spp. in homemade white cheese,ˮ Food Control, vol. 19 no. 4, pp. 360–363, 2008.
[32] T. O. Kevenk and G. T. Gülel. “Prevalence, antimicrobial resistance and serotype distribution of Listeria monocytogenes isolated from raw milk and dairy products,ˮ Journal of Food Safety, vol. 36, no. 1, pp. 11–18, 2016.
[33] C. Poyart-Salmeron, C. Carlier, P. Trieu-Cuot, P. Courvalin and A, Courtieu, “Transferable plasmid-mediated antibiotic resistance in Listeria monocytogenes,ˮ The Lancet, vol. 335, no. 8703, pp. 1422–1426, 1990.
[34] P. J. Slade and D. L. Collins-Thompson, “Listeria plasmids antibiotic resistance and food,ˮ Lancet, vol. 336, no. 8721, pp. 1004, 1990.
[35] B. Facinelli, E. Giovanetti, P. Varaldo, P. Casolari and U. Fabio, “Antibiotic resistance in foodborne Listeria,ˮ Lancet, vol. 338, no. 16, pp. 1272, 1991.
[36] B. Facinelli, M. Roberts, E. Giovanetti, C. Casolari, U. Fabio and P. Varaldo, “Genetic basis of tetracycline resistance in food-borne isolates of Listeria innocua,ˮ Applied and Environmental Microbiology, vol. 59, no. 2, pp. 614–616, 1993.
[37] K. Hadorn, H. Hächler, A. Schaffner and F. Kayser, “Genetic characterization of plasmid-encoded multiple antibiotic resistance in a strain of Listeria monocytogenes causing endocarditisˮ European Journal of Clinical Microbiology and Infectious Diseases, vol. 12, no. 12, pp. 928–937, 1993.
[38] C. F. Abuín, E. Q. Fernández, C. F. Sampayo, J. R. Otero, L. D. Rodríguez and A. C. Sáez, “Susceptibilities of Listeria species isolated from food to nine antimicrobial agents. Antimicrobial agents and chemotherapy,ˮ vol. 38, no. 7, pp. 1655–1657, 1994.
[39] E. Charpentier, G. Gerbaud, C. Jacquet, J. Rocourt and P. Courvalin, “Incidence of antibiotic resistance in Listeria species,ˮ Journal of Infectious Diseases, vol. 172, no. 1, pp. 277–281, 1995.
[40] E. Charpentier and P. Courvalin, “Antibiotic Resistance in Listeria spp. Antimicrobial agents and chemotherapy,ˮ vol. 43, no. 9, pp. 2103–2108, 1999.
[41] A. Aksoy, Ç. Sezer, L. Vatansever and G. Gülbaz, “Presence and Antibiotic Resistance of Listeria monocytogenes in Raw Milk and Dairy Products,ˮ Kafkas Universitesi Veteriner Fakultesi Dergisi, vol. 24, no. 3, pp. 415–421, 2018.
[42] V. Srinivasan, H. Nam, L. Nguyen, B. Tamilselvam, S. Murinda and S. Oliver, “Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms,ˮ Foodbourne Pathogens & Disease, vol. 2, no. 3, pp. 201–211, 2005.
[43] S. Harakeh, I. Saleh, O. Zouhairi, E. Baydoun, E. Barbour and N. Alwan, “Antimicrobial resistance of Listeria monocytogenes isolated from dairy-based food productsˮ Science of the Total Environment, vol. 407, no. 13, pp. 4022–4027, 2009.
[44] H. Jamali, B. Radmehr and K. L. Thong, “Prevalence, characterisation, and antimicrobial resistance of Listeria species and Listeria monocytogenes isolates from raw milk in farm bulk tanks,ˮ Food Control, vol. 34, no. 1, pp. 121–125, 2013.
[45] M. Conter, D. Paludi, E. Zanardi, S. Ghidini, A. Vergara and A. Ianieri, “Characterization of antimicrobial resistance of foodborne Listeria monocytogenes,ˮ International Journal of Food Microbiology, vol. 128, no. 3, pp. 497–500, 2009.
[46] L. O’Connor et al., “The characterization of Listeria spp. isolated from food products and the food‐processing environment,ˮ Letters in Applied Microbiology, vol. 51, no. 5, pp. 490–498, 2010.
[47] D. Walsh, G. Duffy, J. Sheridan, I. Blair and D. McDowell, “Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail foods,ˮ Journal of Applied Microbiology, vol. 90, no. 4, pp. 517–522, 2001.
[48] J. Rocourt, H. Hof, A. Schrettenbrunner, R. Malinverni and J. Bille, “Acute purulent Listeria seelingeri meningitis in an immunocompetent adult,ˮ Schweizerische Medizinische Wochenschrift, vol. 116, no. 8, pp. 248–251, 1986.