Volume 11, Issue 3 (September 2024)                   J. Food Qual. Hazards Control 2024, 11(3): 177-185 | Back to browse issues page

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Varela-Rangel Y, Guillén L, Cuadra-Sánchez C, Araque M. Molecular Typing of Potentially Pathogenic Escherichia coli Isolated from Fresh Pasta Filata Venezuelan Cheeses. J. Food Qual. Hazards Control 2024; 11 (3) :177-185
URL: http://jfqhc.ssu.ac.ir/article-1-1204-en.html
Molecular Microbiology Laboratory, Faculty of Pharmacy and Bioanalysis, University of The Andes, Mérida 5101, Venezuela , araquemc@ula.ve
Abstract:   (101 Views)
Background. Fresh pasta filata cheese is considered as one of the most important foods in the Venezuelan diet. It is typically produced by small-scale producers using raw milk. The objective of this research was to molecularly characterize the pathogenic potential of Escherichia coli strains isolated from pasta filata cheese manufactured and marketed in Venezuela.
Methodology. In the period between January and March of 2019, a total of 36 strains of E. coli were isolated from a variety of pasta filata cheeses including 17 samples of mozzarella, 16 of telita, and 3 of guayanés. These strains were isolated according to the Venezuelan Commission of Industrial Standards (COVENIN) and identified by conventional methods (biochemical and phenotypic tests). Antimicrobial susceptibility was determined using the disk diffusion technique. Phylogenetic grouping and detection of virulence genes were performed by Polymerase Chain Reaction amplification. Diversity and genetic relationships were determined by Rep-PCR.
Results: All strains were susceptible to the tested antibiotics. Phylogroup A (n=19) was the most frequent (52.8%), followed by groups D (n=11; 30.6%), and B1 (n=2; 5.6%). The majority of isolates carried at least two virulence genes, one coding for adhesion mechanisms (fimH) and the other for iron uptake (fyuA). Only one strain of phylogroup A presented a profile consisting of four virulence genes (fimH, fyuA, kpsMT II, and papAH). Four strains that could not be classified according to Clermont's scheme carried resistance genes as well. A heterogeneous population structure was observed by Rep-PCR of the strains.
Conclusion: Results support the hypothesis that the E. coli strains isolated from the three types of pasta filata cheeses manufactured and marketed in Venezuela have identical characteristics and virulence factors to Extraintestinal Pathogenic E. coli strains observed in animals and humans, posing a potential health risk. Therefore, it is essential to improve hygienic and sanitary controls at all stages of cheese production and to implement measures for epidemiological surveillance of potentially pathogenic bacterial strains present in Venezuelan, artisanal pasta filata cheeses.

DOI: 10.18502/jfqhc.11.3.16589
Full-Text [PDF 565 kb]   (71 Downloads)    
Type of Study: Original article | Subject: Special
Received: 24/03/13 | Accepted: 24/09/05 | Published: 24/09/30

References
1. Bagel A., Sergentet D. (2022). Shiga toxin-producing Escherichia coli and milk fat globules. Microorganisms. 10: 496. [DOI: 10.3390/ microorganisms10030496] [DOI:10.3390/microorganisms10030496] [PMID] [PMCID]
2. Beghain J., Bridier-Nahmias A., Le Nagard H., Denamur E., Clermont O. (2018). Clermon typing: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microbial Genomics. 4: e000192. [DOI: 10.1099/mgen.0.000192] [DOI:10.1099/mgen.0.000192] [PMID] [PMCID]
3. Braz V.S., Melchior K., Moreira C.G. (2020). Escherichia coli as a multifaceted pathogenic and versatile bacterium. Frontiers in Cellular and Infection Microbiology. 10: 548492. [DOI: 10.3389/fcimb.2020.548492] [DOI:10.3389/fcimb.2020.548492] [PMID] [PMCID]
4. Bujnáková D., Karahutová L., Kmet V. (2021). Escherichia coli specific virulence-gene markers analysis for quality control of ovine cheese in Slovakia. Microorganisms. 9: 1808. [DOI: 10.3390/microorganisms9091808] [DOI:10.3390/microorganisms9091808] [PMID] [PMCID]
5. Carlos C., Pires M.M., Stoppe N.C., Hachich E.M., Sato M.I., Gomes T.A., Amaral L.A., Ottoboni L.M.M. (2010). Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiology. 10: 161. [DOI: 10.1186/1471-2180-10-161] [DOI:10.1186/1471-2180-10-161] [PMID] [PMCID]
6. Clermont O., Christenson J.K., Denamur E., Gordon D.M. (2013). The Clermont Escherichia coli phylo-typing method revisited: Improvement of specificity and detection of new phylogroups. Environmental Microbiology Reports. 5: 58-65. [DOI: 10.1111/1758-2229.12019] [DOI:10.1111/1758-2229.12019] [PMID]
7. Clinical and Laboratory Standards Institute (CLSI). (2023). Performance standards for antimicrobial susceptibility testing. 33th edition. CLSI Supplement M100-S27, Wayne, Pennsylvaniya. URL: https://clsi.org/standards/products/ microbiology/ documents/m100/. Accessed 03 February 2024.
8. D'Amico D.J. (2014). Microbiological quality and safety issues in cheesemaking. Microbiology Spectrum. 2: CM-0011-2012. [DOI: 10.1128/microbiolspec.CM-0011-2012] [DOI:10.1128/microbiolspec.CM-0011-2012] [PMID]
9. De Campos A.C.L.P., Puño-Sarmiento J.J., Medeiros L.P., Gazal L.E.S., Maluta R.P., Navarro A., Kobayashi R.K.T., Fagan E.P., Nakazato G. (2018). Virulence genes and antimicrobial resistance in Escherichia coli from cheese made from unpasteurized milk in Brazil. Foodborne Pathogens and Disease. 15: 94-100. [DOI: 10.1089/fpd.2017.2345] [DOI:10.1089/fpd.2017.2345] [PMID]
10. Guillén L., Millán B., Araque M. (2014). Molecular characterization of Escherichia coli strains isolated from homemade dairy foods produced in Mérida, Venezuela. Infectio. 18: 100-108. [DOI: 10.1016/j.infect.2014.04.004]. [Spanish with English abstract] [DOI:10.1016/j.infect.2014.04.004]
11. Jakobsen L., Spangholm D.J., Pedersen K., Jensen L.B., Emborg H.D., Agerso Y., Aarestrup F.M., Hammerum A.M., Frimodt-Moller N. (2010). Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Escherichia coli isolates from community-dwelling humans and UTI patients. International Journal of Food Microbiology. 142: 264-272. [DOI: 10.1016/j.ijfoodmicro.2010.06.025] [DOI:10.1016/j.ijfoodmicro.2010.06.025] [PMID]
12. Johnson J.R., Stell A.L. (2000). Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. The Journal of Infectious Diseases. 181: 261-272. [DOI: 10.1086/315217] [DOI:10.1086/315217] [PMID]
13. Koski L., Kisselburgh H., Landsman L., Hulkower R., Howard-Williams M., Salah Z., Kim S., Bruce B.B., Bazaco M.C., Batz M.B., Parker C.C., Leonard C.L., et al. (2022). Foodborne illness outbreaks linked to unpasteurised milk and relationship to changes in state laws - United States, 1998-2018. Epidemiology and Infection. 150: e183. [DOI: 10.1017/S0950268822001649] [DOI:10.1017/S0950268822001649] [PMID] [PMCID]
14. Maldonado Gómez R.J, Rodríguez M., Llanca Córdova L.R., Román Montilla Y.J., Isturiz Vásquez R., Giménez Alfaro O.J., Gámez Mendoza L.A., Meléndez B. (2011). General technological flow diagram and characterization of filata cheese telita type. Agronomía Tropical. 61: 177-188. [Spanish with English abstract]
15. Márquez J.G., García R C.E. (2007). Pathogenic microflora found in white "telita" cheese made in four states of Venezuela. Anales Venezolanos de Nutrición. 20: 17-21. [Spanish with English abstract]
16. Millán Y., Méndez A., Burguera M., Pimentel P., Araque M., Ramírez A. (2018). Determination of enterobacteria and detection of virulence genes in Escherichia coli isolated from raw milk. Revista de la Sociedad Venezolana de Microbiología. 38: 58-63. [Spanish with English abstract]
17. Millán Y., Araque M., Ramírez A. (2020). Distribution of phylogenetic groups, virulence factors and antimicrobial susceptibility in strains of uropathogenic Escherichia coli. Revista Chilena de Infectología. 37: 117-123. [DOI: 10.4067/s0716-10182020000200117]. [Spanish with English abstract] [DOI:10.4067/s0716-10182020000200117] [PMID]
18. Ombarak R.A., Hinenoya A., Awasthi S.P., Iguchi A., Shima A., Elbagory A.R.M., Yamasaki S. (2016). Prevalence and pathogenic potential of Escherichia coli isolates from raw milk and raw milk cheese in Egypt. International Journal of Food Microbiology. 221: 69-76. [DOI: 10/1016/j. ijfoodmicro.2016.01.009] [DOI:10.1016/j.ijfoodmicro.2016.01.009] [PMID]
19. Ovi F., Zhang L., Nabors H., Jia L., Adhikari P. (2023). A compilation of virulence-associated genes that are frequently reported in avian pathogenic Escherichia coli (APEC) compared to other E.coli. Journal of Applied Microbiology. 134: 1-20. [DOI: 10.1093/jambio/lxad014] [DOI:10.1093/jambio/lxad014] [PMID]
20. Perdomo C., Gutiérrez F., García O., Acevedo I., Bastidas Z., Kowalski A. (2015). Physicochemical and bacteriological characterization of white artisan cheese in Buria parish, Lara state, Venezuela. Gaceta de Ciencias Veterinarias. 20: 35-44. [Spanish with English abstract]
21. Pineda A.P.A, Campos G.Z., Pimentel-Filho N.J., Franco B.D.G.d.M., Pinto U.M. (2021). Brazilian artisanal cheeses: diversity, microbiological safety, and challenges for the sector. Frontiers in Microbiology. 12: 666922. [DOI: 10.3389/fmicb.2021.666922] [DOI:10.3389/fmicb.2021.666922] [PMID] [PMCID]
22. Quijada-Martínez P., Flores-Carrero A., Labrador I., Millán Y., Araque M. (2017). Microbiological profile and molecular characterization of multidrug-resistant gram-negative bacilli producing catheter-associated urinary tract infections in the internal medicine services of a Venezuelan university hospital. Austin Journal of Infectious Diseases. 4: 1030.
23. Rodríguez C., Caldas L., Ogeerally P. (2009). Sanitary conditions of hand-made "telita" type cheese in Upata, Bolivar State, Venezuela. Revista de la Sociedad Venezolana de Microbiología. 29: 98-102. [Spanish with English abstract]
24. Sarowska J., Futoma-Koloch B., Jama-Kmiecik A., Frej-Madrzak M., Ksiazczyk M., Bugla-Ploskonska G., Choroszy-Krol I. (2019). Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports. Gut Pathogens. 11: 10. [DOI: 10.1186/s13099-019-0290-0] [DOI:10.1186/s13099-019-0290-0] [PMID] [PMCID]
25. Sebastianski M., Bridger N.A., Featherstone R.M., Robinson J.L. (2022). Diseases outbreaks linked to pasteurized and unpasteurized dairy products in Canada and the United States: a systematic review. Canadian Journal of Public Health. 113: 569-578. [DOI: 10.17269/s41997-022-00614-y] [DOI:10.17269/s41997-022-00614-y] [PMID] [PMCID]
26. Venezuelan Industrial Standards Commission (COVENIN). (1989). Foodstuffs. Identification and sample preparation for microbiological analysis. Standards Nº 1126-89. URL: https://www.scribd.com/doc/50579844/1126-89. Accessed 10 January 2024.
27. Versalovic J., Koeuth T., Lupski J.R. (1991). Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Research. 19: 6823-6831. [DOI: 10.1093/nar/19.24.6823] [DOI:10.1093/nar/19.24.6823] [PMID] [PMCID]

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