Occurrence of Enterococci in the Process of Artisanal Cheesemaking and Their Antimicrobial Resistance
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
APVV-22-0457
Slovak Research and Development Agency
PubMed
39063643
PubMed Central
PMC11277685
DOI
10.3390/life14070890
PII: life14070890
Knihovny.cz E-zdroje
- Klíčová slova
- MALDI-TOF MS, PCR, enterococcal isolates, processing environment, silent genes,
- Publikační typ
- časopisecké články MeSH
Enterococci are a group of microorganisms that have a controversial position from some scientific points of view. The species of the greatest clinical importance are E. faecalis and E. faecium, which are common agents of nosocomial infections. However, enterococci also have important applications in the dairy industry, as they are used as non-starter lactic acid bacteria (NSLAB) in a variety of cheeses, especially artisanal cheeses. The aim of this study was to determine the presence of representatives from the Enterococcus genus using PCR and MALDI-TOF MS methods on samples of raw milk, processing environment swabs, and cheese from four different artisanal dairy plants in Slovakia. Among the 136 isolates of enterococci, 9 species of genus Enterococci (E. faecalis, E. faecium, E. durans, E. devriesi, E. hirae, E. italicus, E. casseliflavus, E. malodoratus, and E. gallinarum) were identified and were tested for their antimicrobial resistance (AMR) to 8 antibiotics (amoxicillin, penicillin, ampicillin, erythromycin, levofloxacin, vancomycin, rifampicin, and tetracycline); most of them were resistant to rifampicin (35.3%), ampicillin (22.8%), and tetracycline (19.9%). A PCR analysis of vanA (4.41%) and tetM (14.71%) revealed that antimicrobial resistance genes were present in not only phenotypic resistant isolates of enterococci but also susceptible isolates. The investigation of antimicrobial resistance in enterococci during the cheesemaking process can be a source of valuable information for public health in the concept of "One Health".
Zobrazit více v PubMed
Švec P., Franz C.M.A.P. Lactic Acid Bacteria: Biodiversity and Taxonomy. In: Holzapfel W.H., Wood B.J.B., editors. The Genus Enterococcus. John Wiley & Sons, Ltd.; Chichester, UK: 2014. 632p
Pilipčinec E., Pistl J., Žilka N., Dorko E., Koščová J., Tkáčiková Ľ., Nemcová R., Segurado B.I. Špeciálna Bakteriológia, Gram-Pozitívne Baktérie. 1st ed. Univerzita Veterinárskeho Lekárstva a Farmácie; Košice, Slovakia: 2019. 328p
Lauková A., Tomáška M., Kmeť V., Strompfová V., Pogány Simonová M., Dvorožňáková E. Slovak local ewe’s milk lump cheese, a source of beneficial Enterococcus durans strain. Food. 2021;10:3091. doi: 10.3390/foods10123091. PubMed DOI PMC
Lauková R., Szabóová P., Pleva P., Buňková L., Chrastinová L. Decarboxylase-positive Enterococcus faecium strains isolated from rabbit meat and their sensitivity to enterocins. Food Sci. Nutr. 2017;5:31–37. doi: 10.1002/fsn3.361. PubMed DOI PMC
Bondi M., Laukova A., De Niederhausern S., Messi P., Papadopoulou C., Economou V. Controversial aspects displayed by enterococci: Probiotics or pathogens? Biomed. Res. Int. 2020;20:e9816185. doi: 10.1155/2020/9816185. PubMed DOI PMC
Silva N., Igrejas G., Gonçalves A., Poeta P. Commensal gut bacteria: Distribution of Enterococcus species and prevalence of Escherichia coli phylogenetic groups in animals and humans in Portugal. Ann. Microbiol. 2012;62:449–459. doi: 10.1007/s13213-011-0308-4. DOI
Silvetti T., Morandi S., Brasca M. Does Enterococcus faecalis from traditional raw milk cheeses serve as a reservoir of antibiotic resistance and pathogenic traits? Foodborne Pathog Dis. 2019;16:359–367. doi: 10.1089/fpd.2018.2542. PubMed DOI
Dapkevicius M.D.L.E., Sgardioli B., Câmara S.P.A., Poeta P., Malcata F.X. Current trends of enterococci in dairy products: A comprehensive review of their multiple roles. Foods. 2021;10:821. doi: 10.3390/foods10040821. PubMed DOI PMC
Graham K., Stack H., Rea R. Safety, beneficial and technological properties of enterococci for use in functional food applications—A review. Crit. Rev. Food Sci. Nutr. 2020;60:3836–3861. doi: 10.1080/10408398.2019.1709800. PubMed DOI
Ogier J.-C., Serror P. Safety assessment of dairy microorganisms: The Enterococcus genus. Int. J. Food Microbiol. 2008;126:291–301. doi: 10.1016/j.ijfoodmicro.2007.08.017. PubMed DOI
Hanchi H., Mottawea W., Sebei K., Hammami R. The genus Enterococcus: Between probiotic potential and safety concerns-an update. Front. Microbiol. 2018;9:1791. doi: 10.3389/fmicb.2018.01791. PubMed DOI PMC
Terzić-Vidojević A., Veljović K., Popović N., Tolinački M., Golić N. Enterococci from raw-milk cheeses: Current knowledge on safety, technological, and probiotic concerns. Foods. 2021;11:2753. doi: 10.3390/foods10112753. PubMed DOI PMC
García-Solache M., Rice L.B. The Enterococcus: A model of adaptability to its environment. Clin. Microbiol. Rev. 2019;32:e00058-18. doi: 10.1128/CMR.00058-18. PubMed DOI PMC
Fiore E., Van Tyne D., Gilmore M.S. Pathogenicity of enterococci. Microbiol. Spectr. 2019:7. doi: 10.1128/microbiolspec.GPP3-0053-2018. PubMed DOI PMC
Różańska H., Lewtak-Piłat A., Osek J. Enterococci—Multifaceted microorganisms. Życie Weter. 2013;88:562–564.
Hollenbeck B.L., Rice L.B. Intrinsic and acquired resistance mechanisms in Enterococcus. Virulence. 2012;3:421–569. doi: 10.4161/viru.21282. PubMed DOI PMC
Microbiology of Food and Animal Feeding Stuffs. Preparation of Test Samples, Initial Suspension and Decimal Dilutions for Microbiological Examination. Part 5 Specific Rules for the Preparation of Milk and Milk Products. Slovak Standards Institute; Bratislava, Slovakia: 2010.
Microbiology of the Food Chain—Horizontal Methods for Surface Sampling. Slovak Standards Institute; Bratislava, Slovakia: 2018.
Hein I., Jorgensen H.J., Loncarevic S., Wagner M. Quantification of Staphylococcus aureus in unpasteurised bovine and caprine milk by real-time PCR. Res. Microbiol. 2005;156:554–563. doi: 10.1016/j.resmic.2005.01.003. PubMed DOI
Ke D., Picard F.J., Martineau F., Ménard C., Roy P.H., Ouellette M., Bergeron M.G. Development of a PCR assay for rapid detection of enterococci. J. Clin. Microbiol. 1999;37:3497–3503. doi: 10.1128/JCM.37.11.3497-3503.1999. PubMed DOI PMC
Martineau F., Picard F.J., Roy P.H., Ouellette M., Bergeron M.G. Species-specific and ubiquitous DNA-based assays for rapid identification of Staphylococcus epidermidis. J. Clin. Microbiol. 1996;34:2888–2893. doi: 10.1128/jcm.34.12.2888-2893.1996. PubMed DOI PMC
Mwikuma G., Kainga H., Kallu S.A., Nakajima C., Suzuki Y., Hang’ombe B.M. Determination of the Prevalence and Antimicrobial Resistance of Enterococcus faecalis and Enterococcus faecium Associated with Poultry in Four Districts in Zambia. Antibiotics. 2023;12:657. doi: 10.3390/antibiotics12040657. PubMed DOI PMC
Brucker Daltonics . MALDI Biotyper 2.0. Software for Microorganism Identification and Classification User Manual. Bruker Scientific LLC; Billerica, MA, USA: 2008.
Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2023. CLSI document M100–S33. Thirty-third Informational Supplement.
European Centre for Disease Prevention and Control European Surveillance of Antimicrobial Consumption Network (ESAC-Net) [(accessed on 31 May 2024)]. Available online: https://www.ecdc.europa.eu/en/about-us/partnerships-and-networks/disease-and-laboratory-networks/esac-net.
European Surveillance of Veterinary Antimicrobial Consumption (ESVAC): 2009–2023. [(accessed on 31 May 2024)]. Available online: https://www.ema.europa.eu/en/veterinary-regulatory-overview/antimicrobial-resistance-veterinary-medicine/european-surveillance-veterinary-antimicrobial-consumption-esvac-2009-2023.
European Committee on Antimicrobial Susceptibility Testing EUCAST Clinical Breakpoint Table. 2023. [(accessed on 31 May 2024)]. Available online: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_14.0_Breakpoint_Tables.pdf.
Výrostková J., Regecová I., Dudriková E., Marcinčák S., Vargová M., Kováčová M., Maľová J. Antimicrobial Resistance of Enterococcus sp. Isolated from Sheep and Goat Cheeses. Foods. 2021;10:1844. doi: 10.3390/foods10081844. PubMed DOI PMC
Dutka-Malen S., Evers S., Courvalin P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clin. Microbiol. 1995;33:24–27. doi: 10.1128/jcm.33.1.24-27.1995. PubMed DOI PMC
Gołaś-Prądzyńska M., Rola J.G. Occurrence and antimicrobial resistance of enterococci isolated from goat’s milk. J. Vet. Res. 2021;65:449–455. doi: 10.2478/jvetres-2021-0071. PubMed DOI PMC
Nafadi H.K.M., Ahmed S.A., Rashwan R.S., Galal S.M., Abd El-Kareem D.M.A., Hamid R.F.A. Molecular Characterization of Antibiotics Resistance Genes of Enterococci Isolated from Raw Milk in Assiut City. Assiut Vet. Med. J. 2023;10:148–159. doi: 10.21608/avmj.2023.221332.1164. DOI
Hamzah A.M., Kadim H.K. Isolation and identification of Enterococcus faecalis from cow milk samples and vaginal swabs from human. J. Entomol. Zool. Stud. 2018;6:218–222.
Fabianová J., Ducková V., Čanigová M., Kročko M. Presence of enterococci in cow milk and their antibiotic resistance. Potravinárstvo. 2010;4:17–21. doi: 10.5219/45. DOI
Bouymajane A., Rhazi F.F., Oulghazi S., Eddra A., Benhallam F., El Allaoui A., Anissi J., Sendide K., Ouhmidou B., Moumni M. Occurrence, molecular and antimicrobial resistance of Enterococcus spp. isolated from raw cow’s milk trade by street trading in Meknes city, Morocco. GERMS. 2018;8:77–84. doi: 10.18683/germs.2018.1134. PubMed DOI PMC
Jamet E., Akary E., Poisson M.A., Chamba J.F., Bertrand X., Serror P. Prevalence and characterization of antibiotic resistant Enterococcus faecalis in French cheeses. Food Microbiol. 2012;31:191–198. doi: 10.1016/j.fm.2012.03.009. PubMed DOI
Gaglio R., Couto N., Marques C., De Fatima Silva Lopes M., Moschetti G., Pomba C., Settanni L. Evaluation of antimicrobial resistance and virulence of enterococci from equipment surfaces, raw materials, and traditional cheeses. Int. J. Food Microbiol. 2016;236:107–114. doi: 10.1016/j.ijfoodmicro.2016.07.020. PubMed DOI
Cattoir V. The multifaceted lifestyle of enterococci: Genetic diversity, ecology and risks for public health. Curr. Opin. Microbiol. 2022;65:73–80. doi: 10.1016/j.mib.2021.10.013. PubMed DOI
Jahansepas A., Sharifi Y., Aghazadeh M., Ahangarzadeh Rezaee M. Comparative analysis of Enterococcus faecalis and Enterococcus faecium strains isolated from clinical samples and traditional cheese types in the Northwest of Iran: Antimicrobial susceptibility and virulence traits. Arch. Microbiol. 2020;202:765–772. doi: 10.1007/s00203-019-01792-z. PubMed DOI
Prichula J., Zvoboda D., Pereira R., Medeiros N., Motta A., Azevedo P., Giordani A., Frazzon A. Antimicrobial susceptibility profile and diversity of Enterococci species isolated from raw milk of buffalo in South Brazil. Periódicos Bras. Em Med. Veterinária Zootec. 2013;20:104–109.
Souza B.D., Pereira R.I., Endres C.M., Frazzon J., Prichula J., Frazzon A.P.G. Resistant enterococci isolated from raw sheep’s milk and cheeses from South region of Brazil. Ciência Rural. 2023;53:e20220288. doi: 10.1590/0103-8478cr20220288. DOI
Ercolini D., Hill P.J., Dodd C.E.R. Bacterial community structure and location in Stilton cheese. Appl. Environ. Microbiol. 2003;69:3540–3548. doi: 10.1128/AEM.69.6.3540-3548.2003. PubMed DOI PMC
Muruzović M.Ž., Mladenović K.G., Žugić-Petrović T.D., Comić L.R. Characterization of lactic acid bacteria isolated from traditionally made Serbian Cheese and evaluation of their antagonistic potential against Enterobacteriaceae. J. Food Process. Preserv. 2018;42:e13577. doi: 10.1111/jfpp.13577. DOI
Idriss S.E., Foltýs V., Tančin V., Kirchnerová K., Tancinova D., Zaujec K. Mastitis Pathogens and Their Resistance Against Antimicrobial Agents in Dairy Cows in Nitra, Slovakia. Slovak J. Anim. Sci. 2014;47:33–38.
Hammad A.M., Aly S.S., Hassan H.A., Abbas N.H., Eltahan A., Khalifa E., Shimamoto T. Occurrence, phenotypic and molecular characteristics of vancomycin-resistant enterococci isolated from retail raw milk in Egypt. Foodborne Pathog. Dis. 2021;19:192–198. doi: 10.1089/fpd.2021.0054. PubMed DOI
Chajęcka-Wierzchowska W., Zadernowska A., Zarzecka U., Zakrzewski A., Gajewska J. Enterococci from ready-to-eat food—Horizontal gene transfer of antibiotic resistance genes and genotypic characterization by PCR melting profile. J. Sci. Food Agric. 2019;99:1172–1179. doi: 10.1002/jsfa.9285. PubMed DOI
Domingos-Lopes M.F.P., Stanton C., Ross P.R., Dapkevicius M.L.E., Silva C.C.G. Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal Pico cheese. J. Food Microbiol. 2017;63:178–190. doi: 10.1016/j.fm.2016.11.014. PubMed DOI
Oruc O., Cetin O., Darilmaz D.O., Yüsekdag Z.N. Determination of the biosafety of potential probiotic Enterococcus faecalis and Enterococcus faecium strains isolated from traditional white cheeses. LWT-Food Sci. Technol. 2021;148:111741. doi: 10.1016/j.lwt.2021.111741. DOI
Morandi S., Silvetti T., Lopreiato V., Piccioli-Cappelli F., Trevisi E., Brasca M. Biodiversity and antibiotic resistance profile provide new evidence for a different origin of enterococci in bovine raw milk and feces. Food Microbiol. 2024;120:104492. doi: 10.1016/j.fm.2024.104492. PubMed DOI
Florez A.B., Vazquez L., Rodríguez J., Mayo B. Directed recovery and molecular characterization of antibiotic resistance plasmids from cheese bacteria. Int. J. Mol. Sci. 2021;22:7801. doi: 10.3390/ijms22157801. PubMed DOI PMC
Al-Sahlany S.T. Production of biodegradable film from soy protein and essential oil of lemon peel and use it as cheese preservative. Basrah J. Agric. Sci. 2017;30:27–35. doi: 10.37077/25200860.2017.40. DOI