Research Article
BibTex RIS Cite

Investigation of the Presence of Listeria monocytogenes in Ready-To-Eat Foods

Year 2020, Volume: 17 Issue: 2, 149 - 155, 27.07.2020
https://doi.org/10.32707/ercivet.760814

Abstract

In this study, it was aimed to investigate the presence of Listeria monocytogenes in ready-to-eat foods retailed in Kayseri and Nigde province of Turkey and to determine the molecular characterization and antibiotic resistance profiles of the detected isolates. For this purpose, 64 cigköfte without meat, 54 mayonnaise based Russian salads and 25 cheese desserts samples were collected from different sales points. Listeria monocytogenes isolation was carried out by conventional method in ready-to-eat food samples. Obtained Listeria spp. isolates were identified by species with the Microbact Listeria 12L Kit. Isolates phenotypically determined as L. monocytogenes were confirmed by Polymerase Chain Reaction (PCR). Clonal relationship of L. monocytogenes isolates were revealed by Enterobacterial Repetitive Intergenic Consensus (ERIC) PCR, and lineage and serotype analyzes were performed by Multiplex PCR (mPCR) methods. Disc diffusion method was used to determine the antibiotic susceptibility profiles of the isolates. In the study, L. monocytogenes was isolated in eight of çiğköfte samples (12.5%) and one of Russian salad samples (1.85%). None of the cheese dessert samples were contaminated with L. monocytogenes. As a result of the ERIC PCR analysis, it was determined that the isolates separated four different type of band profiles. In the Allelespecific oligonucleotide (ASO) PCR analysis performed to determine the lineage of L. monocytogenes isolates, it was revealed that all isolates belong to the Lineage I, and serotyping with mPCR, all isolates were determined as serotype 4b. One of the eight isolates obtained in the study was resistant to ampicillin; one was resistant to meropenem, three to erythromycin and two to trimethoprim/ sulfamethoxazole. Within the study, it was determined that antibiotic resistant L. monocytogenes, can be distributed with ready-to-eat foods and poses serious risks in terms of public health. It is considered that food preservation principles should be taken into consideration and using food safety management systems effectively in the production process of ready-to-eat foods that are highly demanded by the society to prevent possible contaminations after production.

References

  • Amajoud N, Leclercq A, Soriano JM, Bracq-Dieye H, El Maadoudi M, Senhaji NS, Abrini J. Prevalence of Listeria spp. and characterization of Listeria monocytogenes isolated from food products in Tetouan, Morocco. Food Control 2018; 84: 436-41.
  • Border PM, Howard JJ, Plastow GS, Siggens KW. Detection of Listeria species and Listeria monocytogenes using polymerase chain reaction. Lett Appl Microbiol 1990; 11(3): 158-62.
  • Cartwright EJ, Jackson KA, Johnson SD, Graves L.M, Silk BJ, Mahon BE. Listeriosis outbreaks and associated food vehicles, United States, 1998-2008. Emerg Infect Dis 2013; 19: 1-9.
  • Centers for disease control and prevention (CDC). Outbreak of Listeria Infections Final Update. https://www.cdc.gov/listeria/outbreaks/monocytogenes-08-19/index.html. Accessed Date: Mayıs 2020.
  • Charlier C, Perrodeau É, Leclercq A, Cazenave B, Pilmi, B, Henry, Dieye, HB. Clinical features and prognostic factors of listeriosis: the MONALISA national prospective cohort study. The Infect Dis 2017; 17(5): 510-9.
  • Chen Y, Chen M, Wang J, Wu Q, Cheng J, Zhang J, Pang, R. Heterogeneity, Characteristics, and Public Health Implications of Listeria monocytogenes in Ready-to-Eat Foods and Pasteurized Milk in China. Front Microbiol 2020; 11: 642.
  • Doumith M, Buchrieser C, Glaser P, Jacquet C, Martin P. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 2004; 42(8): 3819-22.
  • European Food Safety Authority (EFSA) Panel on Biological Hazards (BIOHAZ). Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA J 2018; 16 (1): p. 5134.
  • Garcia-Vallve S, Palau J, Romeu A. Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis. Mol Biol Evol 1999; 16(9): 1125-34.
  • Ghazzi, M, Porto-Fett AC, Ayaz ND, Ozansoy G, Çufaoğlu G, Goncuoglu M, Stahler LJ. Microbiological characterization of çiğ köfte sold at retail in Ankara, Turkey, and evaluation of selected antimicrobials as ingredients to control foodborne pathogens in çiğ köfte during refrigerated storage. Food control 2018; 84: 138-47.
  • Gökmen M, Akkaya L, Kara R. Balıkesir’de satışa sunulan bazı tüketime hazır gıdalarda Salmonella spp. ve Listeria monocytogenes’in yaygınlığı. Van Vet J 2016; 27(1): 31-6.
  • Gurler Z, Pamuk S, Yildirim Y, Ertas N. The microbiological quality of ready-to-eat salads in Turkey: A focus on Salmonella spp. and Listeria monocytogenes. Int J Food Microbiol 2015; 196: 79-83.
  • Hein I, Klein D, Lehner A, Bubert A, Brandl E, Wagner M. Detection and quantification of the iap gene of Listeria monocytogenes and Listeria innocua by a new real-time quantitative PCR assay. Ress Microbiol 2001; 152: 37-46.
  • International Organization for Standardization (ISO). Microbiology of the food chain-Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. Part 1: Detection method. 2017;11290-1.
  • Jeffers GT, Bruce JL, McDonough PL, Scarlett J, Boor JK, Wiedmann M. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology 2001; 147: 1095-104.
  • Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res 2019; 47(1): 256-9.
  • Mercanoğlu Taban B. Listeria monocytogenes in cig kofte without meat: A novel bulgur ball product. J Food Agric Environ 2012; 10(2): 130-2.
  • Nadon CA, Woodward DL, Young C, Rodgers FG, Wiedmann M. Correlations between molecular subtyping and serotyping of Listeria monocytogenes. J Clin Microbiol 2001; 39: 2704-7.
  • Orsi RH, den Bakker HC, Wiedmann M. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. International J Med Microbiol 2011; 301(2): 79-96.
  • Rantsiou K, Alessandria V, Urso R, Dolci P, Cocolin L. Detection, quantification and vitality of Listeria monocytogenes in food as determined by quantitative PCR. Int J Food Microbiol 2008; 121: 99-105.
  • Schlech W. Foodborne listeriosis. Clin. Infect. Dis 2000; 31: 770-5.
  • The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 2018; 8.1. https://eucast.org/ Accessed Date: August 2018.
  • Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği. Resmî Gazete Sayı: 28157 https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-6-1.pdf. Erişim tarihi: Mayıs 2020.
  • Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucl Acids Res 1991; 19: 6823-31.
  • Ward TJ, Gorski L, Borucki MK, Mandrell RE, Hutchins J, Pupedis K. Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J Bacteriol Res 2004; 186(15): 4994-5002.

Tüketime Hazır Gıdalarda Listeria monocytogenes Varlığının Araştırılması

Year 2020, Volume: 17 Issue: 2, 149 - 155, 27.07.2020
https://doi.org/10.32707/ercivet.760814

Abstract

Bu çalışmada, Kayseri ve Niğde’de perakende olarak satışa sunulan bazı tüketime hazır gıdalarda Listeria monocytogenes varlığının araştırılması, tespit edilen izolatların moleküler karakterizasyonu ve antibiyotik dirençlilik profillerinin belirlenmesi amaçlanmıştır. Bu amaçla farklı dönemlerde olmak üzere farklı satış noktalarından 64 etsiz çiğ köfte, 54 mayonez bazlı Rus salatası ve 25 peynir tatlısı örneği toplanmıştır. Tüketime hazır gıda numunelerinden konvansiyonel yöntemlerle Listeria monocytogenes izolasyonu gerçekleştirilmiştir. Elde edilen Listeria spp. şüpheli izolatlar Microbact Listeria 12L Kit ile tür bazında identifiye edilmiştir. Fenotipik olarak L. monocytogenes olduğu belirlenen izolatlar Polimeraz Zincir Reaksiyonu (PZR) ile doğrulanmıştır. Listeria monocytogenes izolatlarının klonal yakınlıkları Enterobacterial Repetitive Intergenic Consensus (ERIC) PZR ile belirlenmiş, ayrıca Multipleks PZR (mPZR) yöntemi ile nesil ve serotip analizleri gerçekleştirilmiştir. İzolatların antibiyotik duyarlılık profillerinin belirlenmesinde disk difüzyon metodu kullanılmıştır. Çalışma kapsamında etsiz çiğ köfte numunelerinin sekizinden (%12.5) ve Rus salatası örneklerinin ise birinden (%1.85) L. monocytogenes izole edilmiştir. Araştırılan peynir tatlısı örneklerinin hiçbirinde L. monocytogenes tespit edilmemiştir. Yapılan ERIC PZR analizi sonucunda izolatların dört farklı tipte bant profili ortaya koydukları belirlenmiştir. L. monocytogenes izolatlarının nesillerinin belirlenmesi amacıyla yapılan Allelspesifik Oligonükleotid (ASO) PZR analizinde tüm izolatların birinci nesile ait oldukları; mPZR ile yapılan serotiplendirmede ise tüm izolatların 4b serotipi olduğu ortaya konulmuştur. Çalışma kapsamında elde edilen sekiz izolatın birinin ampisiline; birinin meropeneme, üçünün eritromisine ve ikisinin ise trimetoprim/sülfometaksazol’e dirençli oldukları belirlenmiştir. Bu çalışma ile halk sağlığı açısından ciddi riskler oluşturan ve etkin kullanılan antibiyotiklere karşı direnç gösterebilen L. monocytogenes’in tüketime hazır gıdalar aracılığıyla dağılım gösterebileceği belirlenmiştir. Toplum tarafından talep gören tüketime hazır gıdaların üretiminde, gıda güvenliği yönetim sistemlerinin etkin şekilde kullanılması ve üretim sonrasında olası kontaminasyonların önüne geçilmesi amacıyla gıda muhafaza ilkelerinin göz önünde bulundurulması gerekmektedir.

References

  • Amajoud N, Leclercq A, Soriano JM, Bracq-Dieye H, El Maadoudi M, Senhaji NS, Abrini J. Prevalence of Listeria spp. and characterization of Listeria monocytogenes isolated from food products in Tetouan, Morocco. Food Control 2018; 84: 436-41.
  • Border PM, Howard JJ, Plastow GS, Siggens KW. Detection of Listeria species and Listeria monocytogenes using polymerase chain reaction. Lett Appl Microbiol 1990; 11(3): 158-62.
  • Cartwright EJ, Jackson KA, Johnson SD, Graves L.M, Silk BJ, Mahon BE. Listeriosis outbreaks and associated food vehicles, United States, 1998-2008. Emerg Infect Dis 2013; 19: 1-9.
  • Centers for disease control and prevention (CDC). Outbreak of Listeria Infections Final Update. https://www.cdc.gov/listeria/outbreaks/monocytogenes-08-19/index.html. Accessed Date: Mayıs 2020.
  • Charlier C, Perrodeau É, Leclercq A, Cazenave B, Pilmi, B, Henry, Dieye, HB. Clinical features and prognostic factors of listeriosis: the MONALISA national prospective cohort study. The Infect Dis 2017; 17(5): 510-9.
  • Chen Y, Chen M, Wang J, Wu Q, Cheng J, Zhang J, Pang, R. Heterogeneity, Characteristics, and Public Health Implications of Listeria monocytogenes in Ready-to-Eat Foods and Pasteurized Milk in China. Front Microbiol 2020; 11: 642.
  • Doumith M, Buchrieser C, Glaser P, Jacquet C, Martin P. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 2004; 42(8): 3819-22.
  • European Food Safety Authority (EFSA) Panel on Biological Hazards (BIOHAZ). Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA J 2018; 16 (1): p. 5134.
  • Garcia-Vallve S, Palau J, Romeu A. Horizontal gene transfer in glycosyl hydrolases inferred from codon usage in Escherichia coli and Bacillus subtilis. Mol Biol Evol 1999; 16(9): 1125-34.
  • Ghazzi, M, Porto-Fett AC, Ayaz ND, Ozansoy G, Çufaoğlu G, Goncuoglu M, Stahler LJ. Microbiological characterization of çiğ köfte sold at retail in Ankara, Turkey, and evaluation of selected antimicrobials as ingredients to control foodborne pathogens in çiğ köfte during refrigerated storage. Food control 2018; 84: 138-47.
  • Gökmen M, Akkaya L, Kara R. Balıkesir’de satışa sunulan bazı tüketime hazır gıdalarda Salmonella spp. ve Listeria monocytogenes’in yaygınlığı. Van Vet J 2016; 27(1): 31-6.
  • Gurler Z, Pamuk S, Yildirim Y, Ertas N. The microbiological quality of ready-to-eat salads in Turkey: A focus on Salmonella spp. and Listeria monocytogenes. Int J Food Microbiol 2015; 196: 79-83.
  • Hein I, Klein D, Lehner A, Bubert A, Brandl E, Wagner M. Detection and quantification of the iap gene of Listeria monocytogenes and Listeria innocua by a new real-time quantitative PCR assay. Ress Microbiol 2001; 152: 37-46.
  • International Organization for Standardization (ISO). Microbiology of the food chain-Horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. Part 1: Detection method. 2017;11290-1.
  • Jeffers GT, Bruce JL, McDonough PL, Scarlett J, Boor JK, Wiedmann M. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology 2001; 147: 1095-104.
  • Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res 2019; 47(1): 256-9.
  • Mercanoğlu Taban B. Listeria monocytogenes in cig kofte without meat: A novel bulgur ball product. J Food Agric Environ 2012; 10(2): 130-2.
  • Nadon CA, Woodward DL, Young C, Rodgers FG, Wiedmann M. Correlations between molecular subtyping and serotyping of Listeria monocytogenes. J Clin Microbiol 2001; 39: 2704-7.
  • Orsi RH, den Bakker HC, Wiedmann M. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. International J Med Microbiol 2011; 301(2): 79-96.
  • Rantsiou K, Alessandria V, Urso R, Dolci P, Cocolin L. Detection, quantification and vitality of Listeria monocytogenes in food as determined by quantitative PCR. Int J Food Microbiol 2008; 121: 99-105.
  • Schlech W. Foodborne listeriosis. Clin. Infect. Dis 2000; 31: 770-5.
  • The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 2018; 8.1. https://eucast.org/ Accessed Date: August 2018.
  • Türk Gıda Kodeksi Mikrobiyolojik Kriterler Yönetmeliği. Resmî Gazete Sayı: 28157 https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-6-1.pdf. Erişim tarihi: Mayıs 2020.
  • Versalovic J, Koeuth T, Lupski JR. Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucl Acids Res 1991; 19: 6823-31.
  • Ward TJ, Gorski L, Borucki MK, Mandrell RE, Hutchins J, Pupedis K. Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J Bacteriol Res 2004; 186(15): 4994-5002.
There are 25 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Serhat Al This is me

Mukaddes Barel This is me

Adalet Dışhan This is me

Fulden Karadal This is me

Harun Hızlısoy This is me

Nurhan Ertaş Onmaz This is me

Yeliz Yıldırım This is me

Zafer Gönülalan This is me

Publication Date July 27, 2020
Submission Date May 28, 2020
Acceptance Date June 23, 2020
Published in Issue Year 2020 Volume: 17 Issue: 2

Cite

APA Al, S., Barel, M., Dışhan, A., Karadal, F., et al. (2020). Tüketime Hazır Gıdalarda Listeria monocytogenes Varlığının Araştırılması. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 17(2), 149-155. https://doi.org/10.32707/ercivet.760814
AMA Al S, Barel M, Dışhan A, Karadal F, Hızlısoy H, Ertaş Onmaz N, Yıldırım Y, Gönülalan Z. Tüketime Hazır Gıdalarda Listeria monocytogenes Varlığının Araştırılması. Erciyes Üniv Vet Fak Derg. July 2020;17(2):149-155. doi:10.32707/ercivet.760814
Chicago Al, Serhat, Mukaddes Barel, Adalet Dışhan, Fulden Karadal, Harun Hızlısoy, Nurhan Ertaş Onmaz, Yeliz Yıldırım, and Zafer Gönülalan. “Tüketime Hazır Gıdalarda Listeria Monocytogenes Varlığının Araştırılması”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 17, no. 2 (July 2020): 149-55. https://doi.org/10.32707/ercivet.760814.
EndNote Al S, Barel M, Dışhan A, Karadal F, Hızlısoy H, Ertaş Onmaz N, Yıldırım Y, Gönülalan Z (July 1, 2020) Tüketime Hazır Gıdalarda Listeria monocytogenes Varlığının Araştırılması. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 17 2 149–155.
IEEE S. Al, “Tüketime Hazır Gıdalarda Listeria monocytogenes Varlığının Araştırılması”, Erciyes Üniv Vet Fak Derg, vol. 17, no. 2, pp. 149–155, 2020, doi: 10.32707/ercivet.760814.
ISNAD Al, Serhat et al. “Tüketime Hazır Gıdalarda Listeria Monocytogenes Varlığının Araştırılması”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 17/2 (July 2020), 149-155. https://doi.org/10.32707/ercivet.760814.
JAMA Al S, Barel M, Dışhan A, Karadal F, Hızlısoy H, Ertaş Onmaz N, Yıldırım Y, Gönülalan Z. Tüketime Hazır Gıdalarda Listeria monocytogenes Varlığının Araştırılması. Erciyes Üniv Vet Fak Derg. 2020;17:149–155.
MLA Al, Serhat et al. “Tüketime Hazır Gıdalarda Listeria Monocytogenes Varlığının Araştırılması”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, vol. 17, no. 2, 2020, pp. 149-55, doi:10.32707/ercivet.760814.
Vancouver Al S, Barel M, Dışhan A, Karadal F, Hızlısoy H, Ertaş Onmaz N, Yıldırım Y, Gönülalan Z. Tüketime Hazır Gıdalarda Listeria monocytogenes Varlığının Araştırılması. Erciyes Üniv Vet Fak Derg. 2020;17(2):149-55.