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Safety Evaluation of Enterocin Producer Enterococcus sp. Strains Isolated from Traditional Turkish Cheeses Cover

Safety Evaluation of Enterocin Producer Enterococcus sp. Strains Isolated from Traditional Turkish Cheeses

By: MINE AVCI and  BANU ÖZDEN TUNCER  
Open Access
|Jun 2017

References

  1. Barbosa J., P.A. Gibbs and P. Teixeira. 2010. Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control 21: 651–656.10.1016/j.foodcont.2009.10.002
  2. Ben Belgacem Z., H. Abriouel, N. Ben Omar, R. Lucas, M. Martínez-Canamero, A. Gálvez and M. Manai. 2010. Antimicrobial activity, safety aspects, and some technological properties of bacteri-ocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control 21: 462–470.
  3. Bover-Cid S., M. Hugas, M. Izquierdo-Pulido and M.C. VidalCarou. 1999. Amino acid decarboxyllase activity of bacteria isolated from fermented pork sausages. Int. J. Food Microbiol. 66: 185–189.10.1016/S0168-1605(00)00526-2
  4. Brandao A. T., Almeida, E. Munoz-Atieza, C. Torres, G. Igrejas, P.E. Hernández, L.M. Cintas, P. Poeta and C. Herranz. 2010. Antimicrobial activity and occurrence of bacteriocin structural genes in Snterococcus spp. of human and animal origin isolated in Portugal. Arch. Microbiol. 192: 927–936.10.1007/s00203-010-0619-z20821195
  5. Cancilla M.R., I.B. Powell, A.J. Hillier and B.E. Davidson. 1992. Rapid genomic fingerprinting of Lactococcus lactis strains by arbitrarily primed polymerase chain reaction with 32P and fluorescent labels. Appl. Environ. Microbiol. 58: 1772–1775.10.1128/aem.58.5.1772-1775.19921956711622250
  6. Cariolato D., C.Andrighetto and A. Lombardi 2008. Occurrence of virulence factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control 19: 886–892.10.1016/j.foodcont.2007.08.019
  7. Chuang O.N., P.M. Schlievert, C.L. Wells, D.A. Manias and T.J. Tripp. 2009. Multiple functional domains of Enterococcus faecalis aggregation substance Asc10 contribute to endocarditis virulence. Infect. Immun. 77: 539–548.10.1128/IAI.01034-08261226318955479
  8. CLSI. 2012. Clinical and Laboratory Standards Institute, Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard-Eleventh Edition. M02-A11, Vol 32 No. 1.
  9. Cosentino S., G.S. Podda, A. Corda, M.E. Fadda, M. Deplano and M.B. Pisano. 2010. Molecular detection of virulence factors and antibiotic resistance pattern in clinical Enterococcus faecalis strains in Sardinia. J. Prev. Med. Hygiene 51: 31–36.
  10. de las Rivas B., A. Marcobal, A.V. Carrascosa and R. Munoz. 2006. PCR detection of foodborne bacteria producing the biogenic amines histamine, tyramine, putrescine and cadaverine. J. Food Protect. 69: 2509–2514.
  11. Dutka-Malen S., S. Evers and P. Courvalin. 1995. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clinic. Microbiol. 33: 24–27.10.1128/jcm.33.1.24-27.19952278727699051
  12. Eaton T.J. and M.J. Gasson. 2001. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol. 67: 1628–1635.10.1128/AEM.67.4.1628-1635.20019277911282615
  13. Edalatian M.R., M.B.H. Najafi, S.A. Mortazavi, Á. Alegría, S. Delgado, M.R. Bassami and B. Mayo. 2012. Production of bacteriocins by Enterococcus spp. isolated from traditional, Iranian, raw milk cheeses, and detection of their encoding genes. Eur. Food Res. Technol. 234: 789–796.
  14. Edwards U., T. Rogall, H. Blocker, M. Emde and E.C. Bottger. 1989. Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Research 17: 7843–7853.10.1093/nar/17.19.78433348912798131
  15. Franz C.M.A.P., A.B. Muscholl-Silberhorn, N.M.K. Yousif, M. Vancanneyt, J. Swings and W.H. Holzapfel. 2001. Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl. Environ. Microbiol. 67: 4385–4389.10.1128/AEM.67.9.4385-4389.20019317811526054
  16. Franz C.M.A.P., M.E. Stiles, K.H. Schleifer and W.H. Holzapfel. 2003. Enterococci in foods-a conundrum for food safety. Int. J. Food Microbiol. 88: 105–122.10.1016/S0168-1605(03)00174-0
  17. Furlaneto-Maia L., K.R. Rocha, F.C. Henrique, A.Giazzi and M.C. Furlaneto 2014. Antimicrobial resistance in Enterococcus spp. isolated from soft cheese in southern Brazil. Adv. Microbiol. 4: 175–181.10.4236/aim.2014.43023
  18. García-Cano I., C.E. Serrano-Maldonado, M. Olvera-García, E. Delgado-Arciniega, C. Peña-Montes, G. Mendoza-Hernández and M. Quirasco. 2014. Antibacterial activity produced by Enterococcus spp. isolated from an artisanal Mexican dairy product, Cotija cheese. LWT Food Sci. Technol. 59: 26–34.10.1016/j.lwt.2014.04.059
  19. Gaspar F.B., M.T.B. Crespo, and M.F.S. Lopes. 2009. Proposal for a reliable enterococcal cytolysin production assay avoiding apparent incongruence between phenotype and genotype. J. Med. Microbiol. 58: 1122–1124.10.1099/jmm.0.006361-0
  20. Giraffa G. 2002. Enterococci from foods. FEMS Microbiol. Rev. 26(2): 163–171.
  21. Giraffa G. 2003 Functionality of enterococci in dairy products. Int. J. Food Microbiol. 88: 215–222.10.1016/S0168-1605(03)00183-1
  22. Inoğlu Z.N. and Y. Tuncer. 2013. Safety assessment of Enterococcus faecium and Enterococcus faecalis strains isolated from Turkish Tulum Cheese. J. Food Safety 33: 369–377.10.1111/jfs.12061
  23. Javed A., T. Masud, Q. ul Ain, M. Imran and S. Maqsood. 2011. Enterocins of Enterococcus faecium, emerging natural food preservatives. Ann. Microbiol. 61: 699–708.
  24. Kalhotka L., I. Manga, J. Přichystalová, M. Hůlová, M. Vylet?lová and K. Šustová. 2012. Decarboxylase activity test of the genus Enterococcus isolated from goat milk and cheese. Acta Veterinaria Brno 81: 145–151.10.2754/avb201281020145
  25. Khan H., S. Flint and P.L. Yu. 2010. Enterocins in food preservation. Int. J. Food Microbiol. 141: 1–10.10.1016/j.ijfoodmicro.2010.03.00520399522
  26. Komprda T., P. Sladková, E. Petirová, V. Dohnal and R. Burdychová. 2010. Tyrosine- and histidine-decarboxylase positive lactic acid bacteria and enterococci in dry fermented sausages. Meat Sci. 86: 870–877.10.1016/j.meatsci.2010.07.01320696534
  27. Lindenstrauß A.G., M. Pavlovic, A. Bringmann, J. Behr, M.A. Ehrmann and R.F. Vogel. 2011. Comparison of genotypic and phenotypic cluster analyses of virulence determinants and possible role of CRISPR elements towards their incidence in Enterococcus faecalis and Enterococcus faecium. Sys. Appl. Microbiol. 34: 553–560.10.1016/j.syapm.2011.05.00221943678
  28. Lopes M.F.S., A.N. Simões R. Tenreiro, J.J. Marques, M.T.B. Crespo. 2006. Activity and expression of a virulence factor, gelatinase, in dairy enterococci. Int. J. Food. Microbiol. 112: 208–214.
  29. Manolopoulou E., P. Sarantinopoulos, E. Zoidou, A. Aktypis, E. Moschopoulou, I.G. Kandarakis and E.M. Anifantakis. 2003. Evolution of microbial populations during traditional Feta cheese manufacture and ripening. Int. J. Food Microbiol. 82: 153–161.10.1016/S0168-1605(02)00258-1
  30. Martín M., J. Gutiérrez, R. Criado, C. Herranz, L.M. Cintas and P.E. Hernández. 2006. Genes encoding bacteriocins and their expression and potential virulence factors of enterococci isolated from wood pigeons (Columba palumbus). J. Food Protect. 69: 520–531.10.4315/0362-028X-69.3.52016541681
  31. Martin-Platero A.M., E. Valdivia, M. Maqueda and M. Martinez-Bueno. 2009. Characterization and safety evaluation of enterococci isolated from Spanish goats’ milk cheeses. Int. J. Food Microbiol. 132: 24–32.10.1016/j.ijfoodmicro.2009.03.01019375810
  32. Medeiros A.W., R.I. Pereira, D.V. Oliveira, P.D. Martins, P.A. d’Azevedo, S. Van der Sand, J. Frazzon, A.P.G. Frazzon. 2014. Molecular detection of virulence factors among food and clinical Enterococcus faecalis strains in south Brazil. Braz. J. Microbiol. 45(1): 327–332.
  33. Moreno M.R.F., P. Sarantinopoulos, E. Tsakalidou and L. De Vuyst. 2006. The role and application of enterococci in food and health. Int. J. Food Microbiol. 106: 1–24.10.1016/j.ijfoodmicro.2005.06.02616216368
  34. Nes I.F., D.B. Diep and H. Holo. 2007. Bacteriocin diversity in Streptococcus and Enterococcus. J. Bacteriol. 189 (4): 1189–1198.
  35. Özden-Tuncer B., Z. Ay and Y. Tuncer. 2013. Occurrence of enterocin genes, virulence factors and antibiotic resistance in three bacteriocin producer Enterococcus faecium strains isolated from Turkish tulum cheese. Turkish J. Biol. 37: 443–449.
  36. Pesavento G., C. Calonico, B. Ducci, A. Magnanini and A. Lo Nostro. 2014. Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol. 41: 1–7.10.1016/j.fm.2014.01.00824750807
  37. Peters R.P.H., M.A. van Agtmael, S. Gierveld, S.A. Danner, A.B.J. Groeneveld, C.M.J.E. Vandenbroucke-Grauls and P.H.M. Savelkoul. 2007. Quantitative detection of Staphylococcus aureus and Enterococcus faecalis DNA in blood to diagnose bacteremia in patients in the intensive care unit. J. Clinic. Microbiol. 45(11): 3641–3646.10.1128/JCM.01056-07216847617881553
  38. Rehaiem A., Z. Ben Belgacem, M.R. Edalatian, B. Martínez, A. Rodrígez, M. Manaí and N.P. Guerra. 2014. Assessment of potential probiotic properties and multiple bacteriocin encodinggenes of the technological performing strain Enterococcus faecium MMRA. Food Control 37: 343–350.10.1016/j.foodcont.2013.09.044
  39. Reviriego C., T. Eaton, R. Martín, E. Jiménez, L. Fernández, M.J. Gasson and J.M. Rodríguez. 2005. Screening of virulence determinants in Enterococcus faecium strains isolated from breast milk. J. Hum. Lac. 21(2): 131–137.10.1177/089033440527539415886339
  40. Riboldi G.P., J. Frazzon, P.A. Azevdo and A.P.G. Frazoon. 2009. Antimicrobial resistance profile of Enterococcus spp. isolated from food in southern Brazil. Braz. J. Microbiol. 40: 125–128.10.1590/S1517-83822009000100021
  41. Rivas F.P., M.P. Castro, M. Vallejo, E. Marguet and C.A. Campos. 2012. Antibacterial potential of Enterococcus faecium strains isolated from ewes’ milk and cheese. LWT – Food Sci. Technol. 46: 428–436.10.1016/j.lwt.2011.12.005
  42. Semedo T., M. Almeida, M.F. Silva Lopes, J.J. Figueiredo Marques, M.T. Barreto Crespo and R. Tenreiro. 2003. Virulence factors in food, clinical and reference enterococci: a common trait in the genus? Sys. Appl. Microbiol. 26: 13–22.
  43. Singh K.V., S.R. Nallapareddy, J. Sillanpää and B.E. Murray. 2010. Importance of the collagen adhesin Ace in pathogenesis and protection against Enterococcus faecalis experimental endocarditis. PLoS Pathogens 6: 1–13.10.1371/journal.ppat.1000716279874820072611
  44. Sparo M., L. Urbizu, M.V. Solana, G. Pourcel, G. Delpech, A. Confalonieri, M. Ceci and S.F. Sanchez Bruni. 2011. High-level resistance to gentamicin: genetic transfer between Enterococcus faecalis isolated from food of animal origin and human microbiota. Lett. Appl. Microbiol. 54: 119–125.10.1111/j.1472-765X.2011.03182.x22098378
  45. Theppangna W., T. Murase, N. Tokumaru, H. Chikumi, E. Shimizu and K. Otsuki. 2007. Screeening of the enterocin genes and antimicrobial activity against pathogenic bacteria in Enterococcus strains obtained from different origins. J. Vet. Med. Sci. 69(12): 1235–1239.
  46. Tuncer Y. 2009. Some technological properties of phenotypically identified Enterococci Strains isolated from Turkish Tulum cheese. Afr. J. Biotechnol. 8(24): 7008–7016.
  47. Tuncer M., B. Özden Tuncer and Y. Tuncer. 2014 Çiğ sütten izole edilen enterosin B üreticisi Enterococcus faecalis MYE58 suşunun güvenlik değerlendirmesi. Gida/’The Journal of Food39(5): 275-282.
  48. Valenzuela A.S., N.B. Omar, H. Abriouel, R.L. López, E. Ortega, M.M. Cañamero and A. Gálvez. 2008. Risk factors in enterococci isolated from foods in Morocco: Determination of antimicrobial resistance and incidence of virulence traits. Food Chem. Toxic. 46: 2648–2652.10.1016/j.fct.2008.04.02118514994
  49. van Belkum M.J., B.J. Hayema, A. Geis, J. Kok and G. Venema. 1989. Cloning of two bacteriocin genes from a lactococcal bacteriocin plasmid. Appl. Environ. Microbiol. 55: 1187–1191.10.1128/aem.55.5.1187-1191.19891842742757379
  50. Vankerckhoven V., T. Van Autgaerden, C. Vael, C. Lammens, S. Chapelle, R. Rossi, D. Jabes and H. Goossens. 2004. Development of multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in Enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J. Clinic. Microbiol. 42: 4473–4479.
  51. Yogurtcu N.N and Y. Tuncer. 2013 Antibiotic susceptibility patterns of Enterococcus strains isolated from Turkish Tulum cheese. Int. J. Dairy Technol. 66(2): 236–242.10.1111/1471-0307.12014
  52. Yousif N.M.K., P. Dawyndt, H. Abriouel, A. Wijaya, U. Schillinger, M. Vancanneyt, J. Swings, H.A. Dirar, W.H. Holzapfel and C.M.A.P. Franz. 2005. Molecular characterization, technological properties and safety aspects of enterococci from “Hussuwa”, an African fermented sorghum product. J. Appl. Microbiol. 96: 216–228.
  53. Yüceer Ö. and B. Özden Tuncer. 2015. Determination of antibiotic resistance and biogenic amine production of lactic acid bacteria isolated from fermented Turkish sausage (sucuk). J. Food Safety 35: 276–285.10.1111/jfs.12177
DOI: https://doi.org/10.5604/01.3001.0010.7839 | Journal eISSN: 2544-4646 | Journal ISSN: 1733-1331
Language: English
Page range: 223 - 233
Submitted on: Jul 26, 2016
Accepted on: Jan 12, 2017
Published on: Jun 28, 2017
Published by: Polish Society of Microbiologists
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2017 MINE AVCI, BANU ÖZDEN TUNCER, published by Polish Society of Microbiologists
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.