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Genetic Diversity of Enterococci in Bryndza Cheese

  • Roman Dušinský
  • Anna Belicová
  • Libor Ebringer
  • Dušan Jurkovič
  • Lívia Križková
  • Mária Mikulášová
  • Juraj KrajčovičEmail author
Conference paper
Part of the NATO Science for Peace and Security Series A: Chemistry and Biology book series (NAPSA)

Abstract

Enterococci are gram-positive bacteria occurring in a remarkable array of environments. They can be found in soil, food, and water, and make up a significant portion of the normal gut flora of humans and animals. As other bacteria of the gut flora, enterococci can also cause infectious diseases. On the other hand enterococci are used as probiotics to improve the microbial balance of the intestine, or as a treatment for gastroenteritis in humans and animals. So far, 35 species have been proposed for inclusion in the genus Enterococcus considered the most controversial group of lactic acid bacteria. Studies on the microbiota of many traditional cheeses, especially in the Mediterranean countries, have indicated that enterococci play an important role in the ripening of these cheeses, hence contributing to their typical taste and flavour. Adaptability of enterococci to different substrates and growth conditions (low and high temperature, extreme pH, and salinity), allows them to increase in number during milk refrigeration, survive pasteurisation and fermentation. The presence and growth of enterococci in cheeses results in organoleptically unique products, which contribute to the local cuisine and the region’s heritage. Due to interlinked European and worldwide markets, these cheeses are widely distributed and are internationally considered as delicacies. In addition to these technological properties, numerous strains of enterococci associated with cheeses, mainly E. faecium and E. faecalis, produce one or more bacteriocins, and may be considered as protective towards spoilage and pathogenic bacteria. Slovak Bryndza is a natural, white, spreadable cheese manufactured according to the traditional method by milling a lump of matured sheep cheese. The cheese samples were obtained from five different commercial distributors in Slovakia and were taken at three different seasonal intervals. Enterococci are found in high levels; an average value among Bryndza cheese samples ranged between 107 and 108 CFU g−1. Three hundred and eight presumed enterococcal isolates were recovered from Bryndza cheese. All isolates were identified to the species level using phenotypical methods and commercial biochemical sets and by genotypic tools, i.e. polymerase chain reaction (PCR) using ddl genes and repetitive element sequence (GTG)5 in combination with phenylalanyl-tRNA synthase gene (pheS) sequence analysis and by whole-cell protein analysis (SDS-PAGE). Entero­coccal strains were identified as E. faecium, E. durans, E. faecalis, E. italicus, E. casseliflavus, E. gallinarum, E. hirae, and eight strains were members of the species Lactococcus lactis. Of the seven enterococcal species isolated, three of them, E. faecium, E. faecalis and E. durans were present in all samples studied, with E. faecium as the predominant one (50% or more in cheese samples from all producers and seasons as well). Results of biochemical and molecular identification of enterococcal species were in agreement in more than 90%. Since E. faecium was found to be a dominant species in all analyzed Bryndza cheese samples, this species was studied in more details. Pulsed-field gel electrophoresis of macrorestriction fragments (PFGE), (GTG)5-PCR and ERIC-PCR were applied to evaluate genetic diversity within this species. Among 176 E. faecium isolates 82 were plasmid positive. Their plasmid DNA was isolated and digested by EcoRI and HindIII restriction endonucleases. The patterns obtained were compared with those obtained by PFGE, (GTG)5-PCR and ERIC-PCR. Molecular approaches revealed that there is not only a considerable genetic variability among E. faecium isolates among various Bryndza distributors, but even at one distributor at different intervals during 1 year. Plasmid profiling and ERIC-PCR have offered a higher resolution than PFGE and (GTG)5-PCR. PCR was also used for assessment of presence of vanA and vanB genes and virulence determinants gelE, agg and cytolysin genes, namely: cylL L , cylL S , cylM, cylB and cylA. Vancomycin resistance genes vanA and vanB were not detected. Agar plate testing confirmed the sensitivity to vancomycin. Gene gelE, was found in 20 E. faecalis isolates, but only 13 of them showed gelatinase-positive phenotype. Seven isolates had five cytolysin genes, but none of the isolates exhibited a positive haemolytic phenotype. Four isolates possessed the agg gene. All enterococcal isolates from Bryndza cheese were susceptible to ampicillin, streptomycin, gentamicin, vancomycin, and teicoplanin as determined by the disk diffusion method. Resistance rates of enterococcal isolates to rifampicin, erythromycin, ciprofloxacin, and nitrofurantoin were 24%, 26%, 2%, and 1%, respectively. Thirty percent of the E. faecium isolates, 3% of the E. durans isolates, and 12% of the E. faecalis isolates exhibited multidrug resistance. The highest frequency of resistant enterococci was observed in Bryndza produced in winter season. In addition to this, in a close collaboration with clinics, we have shown that application of non-pathogenic E. faecium have an important immunostimulatory and antimutagenic properties and can be a promising method for elimination of pathogenic bacteria in the case of some diseases. Assumption of health benefit effects of Bryndza cheese was confirmed by results of our historically first clinical tests based on a daily consumption of Bryndza cheese during 8 weeks. Statistically significant decrease of total cholesterol and LDL-cholesterol was observed. Since enterococci occur in a remarkable array of environments incl. food and water, are the most abundant Gram-positive cocci in humans (considered at the same time as the most controversial group of lactic acid bacteria) any study of genetic diversity of enterococci could be useful to evaluate their potential risks or benefits.

Keywords

Enterococci cheese PFGE ERIC-PCR (GTG)5-PCR probiotics Bryndza intraspecies variability 

Notes

Acknowledgement

This work was supported by VEGA grants No. 1/1269/04, 1/0114/08, and 1/0132/08, by grant VTP 178/2000, and by grant AV 4/2034/08 from the Ministry of Education of the Slovak Republic.

References

  1. Aarestrup FM, Agerso Y, Gerner-Smidt P, Madsen M, Jensen LB (2000) Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark. Diagn Microbiol Infect Dis 37:127–137PubMedCrossRefGoogle Scholar
  2. Agerbaek M, Gerdes LU, Richelsen B (1995) Hypocholesterolaemic effect of a new fermented milk product in healthy middle-aged men. Eur J Clin Nutr 49:346–352PubMedGoogle Scholar
  3. Agerholm-Larsen L, Raben A, Haulrik N, Haulrik N, Hansen AS, Manders M, Astrup A (2000) Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur J Clin Nutr 54:288–297PubMedCrossRefGoogle Scholar
  4. Allen WD, Lingood MA, Porter P. (1996) Enterococcus organisms and their use as probiotics in alleviating irritable bowel syndrome symptoms. European Patent 0508701 (B1)Google Scholar
  5. Andrighetto C, Knijff E, Lombardi A, Torriani S, Vancanneyt M, Kersters K, Swings J, Dellaglio F (2001) Phenotypic and genetic diversity of enterococci isolated from Italian cheeses. J Dairy Res 68:303–316PubMedCrossRefGoogle Scholar
  6. Arizcun C, Barcina Y, Torre P (1997) Identification and characterization of proteolytic activity of Enterococcus spp. isolated from milk and Roncal and Idiazabal cheese. Int J Food Microbiol 38:17–24PubMedCrossRefGoogle Scholar
  7. Barbier N, Saulnier P, Chachaty E, Dumontier S, Andremont A (1996) Random amplified polymorphic DNA typing versus pulsed-field gel electrophoresis for epidemiological typing of vancomycin-resistant enterococci. J Clin Microbiol 34:1096–1099PubMedGoogle Scholar
  8. Basso A, Goffo A, Rossi G, Conterno N (1994) A preliminary characterization of the microflora of Montasio cheese – Occurrence of galactose fermenting strains in cheese and in natural starter cultures. Mic Aliments Nutri 12:139–144Google Scholar
  9. Battistotti B, Bottazzi V, Vola G (1977) Impiego di Str. faecium, Str. thermophilus e bacilli lattici nella caseificazione del formaggio Fontina. Scienza e Tecnica Lattiero-Casearia 28:331Google Scholar
  10. Belicová A, Križková L, Dobias J, Krajčovič J, Ebringer L (2004) Synergic activity of selenium and probiotic bacterium Enterococcus faecium M-74 against selected mutagens in Salmonella assay. Folia Microbiol 49:301–305CrossRefGoogle Scholar
  11. Belicová A, Križková L, Krajčovič J, Jurkovič D, Sojka M, Dušinský R (2007) Antimicrobial susceptibility of Enterococcus species isolated from Slovak Bryndza Cheese. Folia Microbiol 52:115–119CrossRefGoogle Scholar
  12. Bellomo G, Mangiagli A, Nicastro L, Frigerio G (1980) A controlled doubleblind study of SF68 strain as a new biological preparation for the treatment of diarrhoea in pediatrics. Curr Ther Res 28:927–936Google Scholar
  13. Benyacoub J, Czarnecki-Maulden GL, Cavadini C, Sauthier T, Anderson RE, Schiffrin EJ, von der Weid T (2003) Supplementation of food with Enterococcus faecium (SF68) stimulates immune functions in young dogs. J Nutr 133:1158–1162PubMedGoogle Scholar
  14. Benyacoub J, Perez PF, Rochat F, Saudan KY, Reuteler G, Antille N, Humen M, De Antoni GL, Cavadini C, Blum S, Schiffrin EJ (2005) Enterococcus faecium SF68 enhances the immune response to Giardia intestinalis in mice. J Nutr 135:1171–1176PubMedGoogle Scholar
  15. Bertolami BC, Faludi AA, Batloumi M (1999) Evaluation of the effects of a new fermented milk product (Gaio) on primary hypercholesterolemia. Eur J Clin Nutr 53:97–101PubMedCrossRefGoogle Scholar
  16. Boča M, Vyskočil M, Mikulecký M, Ebringer L, Kolibáš E, Kratochvíľová H, Buzgová D (2004) Complex therapy of chronic hepatic encephalopathy with probiotic: Comparison of two studies (in Slovak). Čas Lék Čes 143:324–328Google Scholar
  17. Bouton Y, Guyot P, Grappin R (1998) Preliminary characterization of microflora of Comte cheese. J Appl Microbiol 85:123–131PubMedCrossRefGoogle Scholar
  18. Buydens P, Debeuckelaere S (1996) Efficacy of SF68 in the treatment of acute diarrhea. A placebo-controlled trial. Scand J Gastroenterol 31:887–891CrossRefGoogle Scholar
  19. Caridi A, Micari P, Foti F, Ramondino D, Sarullo V (2003) Ripening and seasonal changes in microbiological and chemical parameters of the artisanal cheese Caprino d’Aspromonte produced from raw or thermized goat’s milk. Food Microbiol 20:201–209CrossRefGoogle Scholar
  20. Casalta E, Zennaro R (1997) Effect of specific starters on microbiological, biochemical and sensory characteristics of Venaco, a Corsican soft cheese. Sci Aliment 17:79–94Google Scholar
  21. Centeno JA, Cepeda A, Rodríguez-Otero JL, Docampo F (1995) Estudio higienico-sanitario del queso de Arzúa. Alimentaria 33:91–96Google Scholar
  22. Centeno JA, Menendez S, Rodriguez-Otero JL (1996) Main microbial flora present as natural starters in Cebreiro raw cow’s-milk cheese (northwest Spain). Int J Food Microbiol 33:307–313PubMedCrossRefGoogle Scholar
  23. Centeno JA, Menendez S, Hermida M, Rodriguez-Otero JL (1999) Effects of the addition of Enterococcus faecalis in Cebreiro cheese manufacture. Int J Food Microbiol 48:97–111PubMedCrossRefGoogle Scholar
  24. Cetinkaya Y, Falk P, Mayhall CG (2000) Vancomycin-resistant enterococci. Clin Microbiol Rev 13:686–707PubMedCrossRefGoogle Scholar
  25. Chiew YF, Hall LM (1998) Comparison of three methods for the molecular typing of Singapore isolates of enterococci with high-level aminoglycoside resistances. J Hosp Infect 38:223–230PubMedCrossRefGoogle Scholar
  26. Clewell DB (1993) Bacterial sex pheromone-induced plasmid transfer. Cell 73:9–12PubMedCrossRefGoogle Scholar
  27. Coburn PS, Gilmore MS (2003) The Enterococcus faecalis cytolysin: a novel toxin active against eukaryotic and prokaryotic cells. Cell Microbiol 5:661–669PubMedCrossRefGoogle Scholar
  28. Coque TM, Willems RJL, Fortun J, Top J, Diz S, Loza E, Canton R, Baquero F (2005) Population structure of Enterococcus faecium causing bacteremia in a Spanish University Hospital: setting the scene for a future increase in vancomycin resistance? Antimicrob Agents Chemother 49:2693–2700PubMedCrossRefGoogle Scholar
  29. Cosentino S, Pisano MB, Corda A, Fadda ME, Piras C (2004) Genotypic and technological characterization of enterococci isolated from artisanal Fiore Sardo cheese. J Dairy Res 71:444–450PubMedCrossRefGoogle Scholar
  30. Creti R, Imperi M, Bertuccini L, Fabretti F, Orefici G, Di Rosa R, Baldassarri L (2004) Survey for virulence determinants among Ent. faecalis isolated from different sources. J Med Microbiol 53:13–20PubMedCrossRefGoogle Scholar
  31. De Vuyst L, Avonts L, Makras E (2004) Probotics, prebiotics and gut health ( Chap. 17). In: Remacle C, Reusens B (eds) Functional foods, ageing and degenerative disease. Woodhead Publishing, Cambridge, UK
  32. Del Pozo BF, Gaya P, Medina M, Rodriguez-Marin MA, Nuñez M (1988) Changes of microflora of La Serena ewe’s milk cheese during ripening. J Dairy Res 55:449–455CrossRefGoogle Scholar
  33. Delgado S, Delgado T, Mayo B (2002) Technological performance of several Lactococcus and Enterococcus strains of dairy origin in milk. J Food Prot 65:1590–1596PubMedGoogle Scholar
  34. Descheemaeker P, Lammens C, Pot B, Vandamme P, Goossens H (1997) Evaluation of arbitrarily primed PCR analysis and pulsed-field gel electrophoresis of large genomic DNA fragments for identification of enterococci important in human medicine. Int J Syst Bacteriol 47:555–561PubMedCrossRefGoogle Scholar
  35. Descheemaeker P, Leven M, Chapelle S, Lammens C, Hauchecorne M, Wijdooghe M, Vandamme P, Goossens H (2000) Prevalence and molecular epidemiology of glycopeptide-resistant enterococci in Belgian renal dialysis units. J Infect Dis 181:235–241PubMedCrossRefGoogle Scholar
  36. Devoyod JJ (1969) La flore microbienne du fromage de Roquefort. IV Les entérocoques. Lait 49:637–650CrossRefGoogle Scholar
  37. Devriese LA, Pot B, Collins MD (1993) Phenotypic identification of the genus Enterococcus and differentiation of phylogenetically distinct enterococcal species and species groups. J Appl Bacteriol 75:399–408PubMedCrossRefGoogle Scholar
  38. Dicuonzo G, Gherardi G, Lorino G, Angeletti S, Battistoni F, Bertuccini L, Creti R, Di Rosa R, Venditti M, Baldassarri L (2001) Antibiotic resistance and genotypic characterization by PFGE of clinical and environmental isolates of enterococci. FEMS Microbiol Lett 201:205–211PubMedCrossRefGoogle Scholar
  39. Domig KJ, Mayer HK, Kneifel W (2003) Methods used for the isolation, enumeration, characterization and identification of Enterococcus spp. 2. Pheno- and genotypic criteria. Int J Food Microbiol 88:165–188PubMedCrossRefGoogle Scholar
  40. Donabedian SM, Chow JW, Boyce JM, McCabe RE, Markowitz SM, Coudron PE, Kuritza A, Pierson CL, Zervos MJ (1992) Molecular typing of ampicillin-resistant, non-ß-lactamase-producing Enterococcus faecium isolates from diverse geographic areas. J Clin Microbiol 30:2757–2761PubMedGoogle Scholar
  41. Drahovská H, Kocíncová D, Seman M, Turna J (2002) PCR-based methods for identification of Enterococcus species. Folia Microbiol 47:649–653CrossRefGoogle Scholar
  42. Drahovská H, Slobodníková L, Kocincová D, Seman M, Končeková R, Trupl J, Turňa J (2004) Antibiotic resistance and virulence factors among clinical and food enterococci isolated in Slovakia. Folia Microbiol 49:763–768CrossRefGoogle Scholar
  43. Duthoit F, Godon JJ, Montel MC (2003) Bacterial community dynamics during production of registered designation of origin Salers cheese as evaluated by 16S rRNA gene single-strand conformation polymorphism analysis. Appl Environ Microbiol 69:3840–3848PubMedCrossRefGoogle Scholar
  44. Dutka-Malen S, Evers S, Courvalin P (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J Clin Microbiol 33:24–27PubMedGoogle Scholar
  45. Eaton TJ, Gasson MJ (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol 67:1628–1635PubMedCrossRefGoogle Scholar
  46. Ebringer L, Ferenčík M, Lahitová N, Kačani L, Michalková D (1995) Antimutagenic and immunostimulatory properties of lactic acid bacteria. World J Microbiol Biotechnol 11:294–298CrossRefGoogle Scholar
  47. Elsner HA, Sobottka I, Mack D, Claussen M, Laufs R, Wirth R (2000) Virulence factors of Enterococcus faecalis and Enterococcus faecium blood culture isolates. Eur J Clin Microbiol Infect Dis 19:39–42PubMedCrossRefGoogle Scholar
  48. Engelbert M, Mylonakis E, Ausubel FM, Calderwood SB, Gilmore MS (2004) Contribution of gelatinase, serine protease, and fsr to the pathogenesis of Enterococcus faecalis endophthalmitis. Infect Immun 72:3628–3633PubMedCrossRefGoogle Scholar
  49. Ennahar S, Aoude-Werner D, Assobhei O, Hasselmann C (1998) Antilisterial activity of enterocin 81, a bacteriocin produced by Enterococcus faecium WHE 81 isolated from cheese. J Appl Microbiol 85:521–526PubMedCrossRefGoogle Scholar
  50. Ewing W, Haresign W (1989) Probiotics UK. Chalcombe Publications, Bucks, UKGoogle Scholar
  51. Facklam R, Elliot JA (1995) Identification, classification, and clinical relevance of catalase-negative, Gram-positive cocci, excluding the streptococci and enterococci. Clin Microbiol Rev 8:479–495PubMedGoogle Scholar
  52. Fan Y, Chen S, Yu Y (2006) A probiotic treatment containing Lactobacillus, Bifidobacterium and Enterococcus improves IBS symptoms in an open label trial. Z Zhejiang Univ Sci B7:987–991CrossRefGoogle Scholar
  53. Ferenčík M, Ebringer L, Mikeš Z, Jahnová E, Čižnár I (1999) Beneficial modification of the human intestinal microflora using orally administered lactic acid bacteria (in Slovak). Bratisl Lek Listy 100:238–245PubMedGoogle Scholar
  54. Fines M, Perichon B, Reynolds P, Sahm DF, Courvalin P (1999) Courvalin, VanE, a new type of acquired glycopeptide resistance in Enterococcus faecalis BM4405. Antimicrob Agents Chemother 43:2161–2174PubMedGoogle Scholar
  55. Fontecha J, Pelaez C, Juarez M, Requena T, Gomez C (1990) Biochemical and microbiological characteristics of artisanal hard goat’s cheese. J Dairy Res 73:1150–1157CrossRefGoogle Scholar
  56. Foulquie-Moreno MR, Callewaert R, Devreese B, Van Beeumen J, De Vuyst L (2003) Isolation and biochemical characterisation of enterocins produced by enterococci from different sources. J Appl Microbiol 94:214–229PubMedCrossRefGoogle Scholar
  57. Foulquie-Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L (2006) The role and application of enterococci in food and health. Int J Food Microbiol 106:1–24PubMedCrossRefGoogle Scholar
  58. Franz CMAP, Holzapfel WH, Stiles ME (1999) Enterococci at the crossroads of food safety? Int J Food Microbiol 47:1–24PubMedCrossRefGoogle Scholar
  59. Franz CMAP, Muscholl-Silberhorn AB, Yousif NMK, Vancanneyt M, Swings J, Holzapfel WH (2001) Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol 67:4385–4389PubMedCrossRefGoogle Scholar
  60. Franz CMAP, Stiles ME, Schleifer KH, Holzapfel WH (2003) Enterococci in foods — a conundrum for food safety. Int J Food Microbiol 88:105–122PubMedCrossRefGoogle Scholar
  61. Franzetti L, Pompei M, Scarpellini M, Galli A (2004) Phenotypic and genotypic characterization of Enterococcus spp. of different origins. Curr Microbiol 49:225–260CrossRefGoogle Scholar
  62. Freitas AC, Pais C, Malcata FX, Hogg TA (1996) Microbiological characterization of Picante da Beira Baixa cheese. J Food Prot 59:155–160Google Scholar
  63. Galli D, Wirth R, Wanner G (1989) Identification of aggregation substances of Enterococcus faecalis cells after induction by sex pheromones. An immunological and ultrastructural investigation. Arch Microbiol 151:486–490PubMedCrossRefGoogle Scholar
  64. García MC, Rodríguez MJ, Bernardo A, Tornadijo ME, Carballo J (2002) Study of enterococci and micrococci isolated throughout manufacture and ripening of San Simón cheese. Food Microbiol 19:23–33CrossRefGoogle Scholar
  65. Gardini F, Martuscelli M, Caruso MC, Galgano F, Crudele MA, Favati F, Guerzoni ME, Suzzi G (2001) Effects of pH, temperature and NaCl concentration on growth kinetics, proteolytic activity and biogenic amine production of Enterococcus faecalis. Int J Food Microbiol 64:105–117CrossRefGoogle Scholar
  66. Gelsomino R, Vancanneyt M, Cogan TM, Condon S, Swings J (2002) Source of enterococci in a farmhouse raw-milk cheese. Appl Environ Microbiol 68:3560–3565PubMedCrossRefGoogle Scholar
  67. Gelsomino R, Vancanneyt M, Condon S, Swings J, Cogan TM (2001) Enterococcal diversity in the environment of an Irish Cheddar-type cheesemaking factory. IntJ Food Microbiol 71:177–188PubMedCrossRefGoogle Scholar
  68. Gevers D, Huys G, Swings J (2001) Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol Lett 205:31–36PubMedCrossRefGoogle Scholar
  69. Gilmore MS, Segarra RA, Booth MC (1990) An HlyB-type function is required for expression of the Enterococcus faecalis hemolysin/bacteriocin. Infect Immun 58:3914–3923PubMedGoogle Scholar
  70. Gilmore MS, Segarra RA, Booth MC, Bogie CP, Hall LR, Clewell DB (1994) Genetic structure of the Enterococcus faecalis plasmid pAD1-encoded cytolytic toxin system and its relationship to lantibiotic determinants. J Bacteriol 176:7335–7344PubMedGoogle Scholar
  71. Giraffa G (2002) Enterococci from food. FEMS Microbiol Lett 26:163–171CrossRefGoogle Scholar
  72. Giraffa G (2003) Functionality of enterococci in dairy products. Int J Food Microbiol 88:215–222PubMedCrossRefGoogle Scholar
  73. Giraffa G, Carminati D, Neviani E (1997) Enterococci isolated from dairy products: a review of risks and potential technological use. J Food Prot 60:732–738Google Scholar
  74. Giraffa G, Picchioni N, Neviani E, Carminati D (1995) Production and stability of an Enterococcus faecium bacteriocin during Taleggio cheesemaking and ripening. Food Microbiol 12:301–307CrossRefGoogle Scholar
  75. Godfree AF, Kay D, Wyer D (1997) Faecal streptococci as indicators of faecal contamination in water. Soc Appl Bacteriol Symp Ser 26:110S–119SPubMedCrossRefGoogle Scholar
  76. Goh SH, Facklam RR, Chang M, Hill JE, Tyrrell GJ, Burns EC, Chan D, He C, Rahim T, Shaw C, Hemmingsen SM (2000) Identification of Enterococcus species and phenotypically similar Lactococcus and Vagococcus species by reverse checkerboard hybridization to chaperonin 60 gene sequences. J Clin Microbiol 38:3953–3959PubMedGoogle Scholar
  77. Gordillo ME, Sigh KV, Murray BE (1993) Comparison of ribotyping and pulsed-field gel electrophoresis for subspecies differentiation of strains of Enterococcus faecalis. J Clin Microbiol 31:1570–1574PubMedGoogle Scholar
  78. Hamilton-Miller J, Shah S, Smith CT (1996) Probiotic remedies are not what they seem. BMJ 312:55–56PubMedCrossRefGoogle Scholar
  79. Harwood VJ, Delahoya NC, Ulrich RM, Kramer MF, Whitlock JE, Garey JR, Lim DV (2004) Molecular confirmation of Enterococcus faecalis and E. faecium from clinical, faecal and environmental sources. Lett Appl Microbiol 38:476–482PubMedCrossRefGoogle Scholar
  80. Hlivak P, Odraška J, Ferenčík M, Ebringer L, Jáhnová E, Mikeš Z (2005) One year application of probiotic strain Enterococcus faecium M74 decreases serum cholesterol levels. Bratisl Lek Listy 106:67–72PubMedGoogle Scholar
  81. Hlubinová K, Rychlý B, Altanerová V, Ebringer L, Altaner Č (2004) Influence of diet containing lyophilized Enterococcus faeciumM-74 with organic selenium on tumor incidence in Apc 1638N mice. Neoplasma 51:341–344PubMedGoogle Scholar
  82. Homan WL, Tribe D, Poznanski S, Li M, Hogg G, Spalburg E, Van Embden JD, Willems RJ (2002) Multilocus sequence typing scheme for Enterococcus faecium. J Clin Microbiol 40:1963–1971PubMedCrossRefGoogle Scholar
  83. Hufnagel M, Hancock LE, Koch S, Theilacker C, Gilmore MS, Huebner J (2004) Serological and genetic diversity of capsular polysaccharides in Enterococcus faecalis. J Clin Microbiol 42:2548–2557PubMedCrossRefGoogle Scholar
  84. Huycke MM, Spiegel CA, Gilmore MS (1991) Bacteremia caused by hemolytic, high-level gentamicin-resistant Enterococcus faecalis. Antimicrob Agents Chemother 35:1626–1634PubMedCrossRefGoogle Scholar
  85. Ike Y, Hashimoto H, Clewell DB (1984) Hemolysin of Streptococcus faecalis subspecies zymogenes contributes to virulencein mice. Infect Immun 45:528–530PubMedGoogle Scholar
  86. Ike Y, Hashimoto H, Clewell DB (1987) High incidence of hemolysin production by Enterococcus (Streptococcus) faecalis strains associated with human parenteral infections. J Clin Microbiol 25:1524–1528PubMedGoogle Scholar
  87. Jackson CR, Fedorka-Cray PJ, Barrett JB (2004) Use of a genus- and species-specific multiplex PCR for identification of enterococci. J Clin Microbiol 42:3558–3565PubMedCrossRefGoogle Scholar
  88. Jett BD, Huycke MM, Gilmore MS (1994) Virulence of enterococci. Clin Microbiol Rev 7:462–478PubMedGoogle Scholar
  89. Jurkovič D, Križková L, Dušinský R, Belicová A, Sojka M, Krajčovič J, Ebringer L (2006a) Identification and characterization of enterococci from bryndza cheese. Lett Appl Microbiol 42:553–559PubMedGoogle Scholar
  90. Jurkovič D, Križková L, Sojka M, Belicová A, Dušinský R, Krajčovič J, Snauwaert C, Naser S, Vandamme P, Vancanneyt M (2006b) Molecular identification and diversity of enterococci isolated from slovak bryndza cheese. J Gen Appl Microbiol 52:329–337PubMedCrossRefGoogle Scholar
  91. Jurkovič D, Križková L, Sojka M, Takáčová M, Dušinský R, Krajčovič J, Vandamme P, Vancanneyt M (2007) Genetic diversity of Enterococcus faecium isolated from bryndza cheese. Int J Food Microbiol 116:82–87PubMedCrossRefGoogle Scholar
  92. Kayaoglu G, Orstavik D (2004) Virulence factors of Enterococcus faecalis: relationship to endodontic disease. Crit Rev Oral Biol Med 15:308–320PubMedCrossRefGoogle Scholar
  93. Kayser FH (2003) Safety aspects of enterococci from the medical point of view. Int J Food Microbiol 88:255–262PubMedCrossRefGoogle Scholar
  94. Ke D, Picard FJ, Martineau F, Ménard Ch, Roy PH, Ouellette M, Bergeron MG (1999) Development of a PCR assay for rapid detection of enterococci. J Clin Microbiol 37:3497–3503PubMedGoogle Scholar
  95. Keresteš J, Selecký J (2003) Slovak bryndza cheese. In: Keresteš, J (ed) Dairy industry in Middle Slovakia, pp 109–122. Eminent, Považská Bystrica, SlovakGoogle Scholar
  96. Klein G (2003) Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. Int J Food Microbiol 88:123–131PubMedCrossRefGoogle Scholar
  97. Kuhn I, Burman LG, Haeggman S, Tullus K, Murray BE (1995) Biochemical fingerprinting compared with ribotyping and pulsed-field gel electrophoresis of DNA for epidemiological typing of enterococci. J Clin Microbiol 33:2812–2817PubMedGoogle Scholar
  98. Kumada M, Senpuku H, Motegi M, Nkao R, Yonezawa H, Yamamura H, Watanabe H, Tagami J (2008) Effects of Enterococcus faecium on Streptococcus mutans biofilm formation using flow cell system. J Oral Biosci 50:68–76CrossRefGoogle Scholar
  99. Lauková A, Czikková S (1999) The use of enterocin CCM 4231 in soy milk to control the growth of Listeria monocytogenes and Staphylococcus aureus. J Appl Microbiol 87:182–186PubMedCrossRefGoogle Scholar
  100. Lauková A, Czikková S (2001) Antagonistic effect of enterocin CCM 4231 from Enterococcus faecium on “bryndza”, a traditional Slovak dairy product from sheep milk. Microbiol Res 156:31–34PubMedCrossRefGoogle Scholar
  101. Laurenčik M, Sulo P, Slavikova E, Pieckova E, Seman M, Ebringer L (2008) The diversity of eukaryotic microbiota in the traditional Slovak sheep cheese – Bryndza. Int J Food Microbiol 127:176–179PubMedCrossRefGoogle Scholar
  102. Leclercq R (1997) Enterococci acquire new kinds of resistance. Clin Infect Dis 24:S80–S84PubMedCrossRefGoogle Scholar
  103. Ledda A, Scintu MF, Pirisi A, Sanna S, Mannu L (1994) Technological characterization of lactococci and enterococci for the manufacture of Fiore Sardo sheep cheese. Scienza e Tecnica Lattiero-Casearia 45:443–456Google Scholar
  104. Litopolou-Tzanetaki E (1990) Changes in numbers and kinds of lactic acid bacteria during ripening of Kefalotyri cheese. J Food Sci 55:111–113CrossRefGoogle Scholar
  105. Litopolou-Tzanetaki E, Tzanetakis N, Vafopoulou-Mastrojiannaki A (1993) Effect of type of lactic starter on microbiological chemical and sensory characteristics of feta cheese. Food Microbiol 10:31–41CrossRefGoogle Scholar
  106. Liu D, Wang C, Swiatlo EJ, Lawrence ML (2005) PCR amplification of a species-specific putative transcriptional regulator gene reveals the identity of Enterococcus faecalis. Microbiol Res 156:944–948CrossRefGoogle Scholar
  107. Loguercio C, Abbiati R, Rinaldi M, Romano A, Vecchio D, Blanco C, Coltorti M (1995) Long-term effects of Enterococcus faecium SF68 versus lactulose in the treatment of patients with cirrhosis and grade 1-2 hepatic encephalopathy. J Hepatol 23:39–46PubMedCrossRefGoogle Scholar
  108. Lopes MFS, Ribeiro T, Abrantes M, Marques JJF, Tenreiro R, Crespo MTB (2005) Antimicrobial resistance profiles of dairy and clinical isolates and type strains of enterococci. Int J Food Microbiol 103:191–198CrossRefGoogle Scholar
  109. Macedo AC, Malcata FX, Hogg TA (1995) Microbiological profile in Serra ewe’s cheese during ripening. J Appl Microbiol 79:1–11CrossRefGoogle Scholar
  110. Maisnier-Patin S, Forni E, Richard J (1996) Purification, partial characterisation and mode of action of enterococcin EFS2, an antilisterial bacteriocin produced by a strain of Enterococcus faecalis isolated from a cheese. Int J Food Microbiol 30:255–270PubMedCrossRefGoogle Scholar
  111. Majhenič AČ, Rogelj I, Perko B (2005) Enterococci from Tolmic cheese: Population structure, antibiotic susceptibility and incidence of virulence determinants. Int J Food Microbiol 102:239–244CrossRefGoogle Scholar
  112. Mannu L, Paba A (2002) Genetic diversity of lactococci and enterococci isolated from home-made Pecorino Sardo ewes’ milk cheese. J Appl Microbiol 92:55–62PubMedCrossRefGoogle Scholar
  113. Mannu L, Paba A, Pes M, Floris R, Scintu MF, Morelli L (1999) Strain typing among enterococci isolated from home-made Pecorino Sardo cheese. FEMS Microbiol Lett 170:25–30PubMedCrossRefGoogle Scholar
  114. Manolopoulou E, Sarantinopoulos P, Zoidou E, Aktypis A, Moschopoulou E, Kandarakis IG, Anifantakis EM (2003) Evolution of microbial populations during traditional Feta cheese manufacture and ripening. Int J Food Microbiol 82:153–161PubMedCrossRefGoogle Scholar
  115. Marino M, Maifreni M, Rondinini G (2003) Microbiological characterization of artisanal Montasio cheese: analysis of its indigenous lactic acid bacteria. FEMS Microbiol Lett 229:133–140PubMedCrossRefGoogle Scholar
  116. Mego M, Ebringer L, Drgoňa L, Mardiak J, Trupl J, Greksak R, Nemová I, Oravcová E, Zajac V, Koza I (2005a) Prevention of febrile neutropenia in cancer patients by probiotic strain Enterococcus faecium M-74. Pilot study phase I. Neoplasma 52:76–80Google Scholar
  117. Mego M, Končeková R, Mikušková E, Drgoňa L, Ebringer L, Demitrovičová L, Nemová I, Trupl J, Mardiak J, Koza I, Zajac V (2006) Prevention of febrile neutropenia in cancer patients by probiotic strain of Enterococcus faecium M-74. Phase II study. Supp Care Cancer 14:285–290CrossRefGoogle Scholar
  118. Mego M, Májek J, Končeková R, Ebringer L, Čierniková S, Rauko P, Kováč M, Trupl J, Slezák P, Zajac V (2005b) Intramucosal bacteria in colon cancer and their elimination by probiotic strain Enterococcus faecium M-74 with organic selenium. Folia Microbiol 50:443–447CrossRefGoogle Scholar
  119. Menéndez S, Godínez R, Centeno JA, Rodríguez-Otero JL (2001) Microbiological, chemical and biochemical characteristics of “Tetilla” raw cows-milk cheese. Food Microbiol 18:151–158CrossRefGoogle Scholar
  120. Mikeš Z, Ebringer L, Boča M, Dušinský R, Jahnová E (2005) Some cardiovascular factors after consumption of the traditional Slovak bryndza cheese – pilot study (in Slovak). Geriatria 1:29–36Google Scholar
  121. Mikeš Z, Ferenčík M, Jahnová E, Ebringer L, Čižnár I (1995) Hypocholesterolemic and immunostimulatory effects of orally applied Enterococcus faecium M-74 in man. Folia Microbiol 40:639–646CrossRefGoogle Scholar
  122. Monstein HJ, Quednau M, Samuelsson A, Ahrné S, Isaksson B, Jonasson J (1998) Division of the genus Enterococcus into species groups using PCR-based molecular typing methods. Microbiology 144:1171–1179PubMedCrossRefGoogle Scholar
  123. Morea M, Baruzzi F, Cocconcelli PS (1999) Molecular and physiological characterization of dominant bacterial populations in traditional Mozzarella cheese processing. J Appl Microbiol 87:574–582PubMedCrossRefGoogle Scholar
  124. Mundy LM, Sahm DF, Gilmore MS (2000) Relationships between enterococcal virulence and antimicrobial resistance. Clin Microbiol Rev 13:513–522PubMedCrossRefGoogle Scholar
  125. Murray BE (1990) The life and times of the Enterococcus. Clin Microbiol Rev 3:46–65PubMedGoogle Scholar
  126. Murray BE, Singh KV, Heath JD, Sharma BR, Weinstock GM (1990) Comparison of genomic DNAs of different enterococcal isolates using restriction endonucleases with infrequent recognition sites. J Clin Microbiol 28:2059–2063PubMedGoogle Scholar
  127. Nallapareddy SR, Qin X, Weinstock GM, Höök M, Murray BE (2000) Enterococcus faecalis adhesin, ace, mediates attachment to extracellular matrix proteins collagen type IV and laminin as well as collagen type I. Infect Immun 68:5218–5224PubMedCrossRefGoogle Scholar
  128. Naser S, Thompson FL, Hoste B, Gevers D, Vandemeulebroecke K, Cleenwerck I, Thompson CC, Vancanneyt M, Swings J (2005) Phylogeny and identification of enterococci by atpA gene sequence analysis. J Clin Microbiol 43:2224–2230PubMedCrossRefGoogle Scholar
  129. NCCLS (2003) National Committee for Clinical Laboratory Standards Document M100-S13: Performance standards for antimicrobial susceptibility testing. 13th Informational Supplement NCCLS, Villanova, PAGoogle Scholar
  130. Núñez M, Rodríguez JL, García E, Gaya P, Medina M (1997) Inhibition of Listeria monocytogenes by enterocin 4 during the manufacture and ripening of Manchego cheese. J Appl Microbiol 83:671–677PubMedCrossRefGoogle Scholar
  131. Ordoñez JA, Barneto R, Ramos M (1978) Studies on Manchego cheese ripened in olive oil. Milchwissenschaft 33:609–612Google Scholar
  132. Ozawa Y, Courvalin P, Gaiimand M (2000) Identification of enterococci at the species level by sequencing of the genes for D-alanine: D-alanine ligases. Sys Appl Microbiol 23:230–237CrossRefGoogle Scholar
  133. Papageorgiou DK, Abrahim A, Bori M, Doundounakis S (1998) Chemical and bacteriological characteristics of Pichtogalo Chanion cheese and mesophilic starter cultures for its production. J Food Prot 61:688–692PubMedGoogle Scholar
  134. Parente E, Villani F, Coppola R, Coppola S (1989) A multiple strain starter for water-buffalo Mozzarella cheese manufacture. Lait 69:271–279CrossRefGoogle Scholar
  135. Patel R, Piper KE, Rouse MS, Steckelberg JM, Uhl JR, Kohner P, Hopkins MK, Cockerill FR, Kline BC (1998) Determination of 16S rRNA sequences of enterococci and application to species identification of nonmotile Enterococcus gallinarum isolates. J Clin Microbiol 36:3399–3407PubMedGoogle Scholar
  136. Perichon B, Reynolds P, Courvalin P (1997) VanD-type glycopeptide-resistant Enterococcus faecium BM4339. Antimicrob Agents Chemother 41:2016–2018PubMedGoogle Scholar
  137. Perlada DE, Smulian AG, Cushion MT (1997) Molecular epidemiology and antibiotic susceptibility of enterococci in Cincinnati, Ohio: a prospective citywide survey. J Clin Microbiol 35:2342–2347PubMedGoogle Scholar
  138. Peters J, Mac K, Wichmann-Schauer H, Klein G, Ellerbroek L (2003) Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany. Int J Food Microbiol 88:311–314PubMedCrossRefGoogle Scholar
  139. Pintado ME, Santos CC, Malcata FX (2001) Activity of adventitious Enterococcus strains on model curdled caprine milk: microbial growth and evolution of concentration of organic acids and lactose throughout time. Meded Rijksuniv Gent Fak Landbouwkd Toegep Biol Wet 66:613–616PubMedGoogle Scholar
  140. Pollmann M, Nordhoff M, Pospischil A, Tedin K, Wieler LH (2005) Effect of a probiotic strain of Enterococcus faecium on the rate of natural chlamydia infection in swine. Infect Immun 73:4346–4353PubMedCrossRefGoogle Scholar
  141. Poyart C, Quesnes G, Trieu-Cuot P (2000) Sequencing the gene encoding Manganese Dependant superoxyde dismutase for rapid species identification of enterococci. J Clin Microbiol 38:415–418PubMedGoogle Scholar
  142. Poznanski E, Cavazza A, Cappa F, Cocconcelli PS (2004) Indigenous raw milk microbiota influences the bacterial development in traditional cheese from an alpine natural park. Int J Food Microbiol 92:141–151PubMedCrossRefGoogle Scholar
  143. Prodromou K, Thasitou P, Haritonidou E, Tzanetakis N, Litopoulou-Tzanetaki E (2001) Microbiology of “Orinotyri” a ewe’s milk cheese from the Greek mountains. Food Microbiol 18:319–328CrossRefGoogle Scholar
  144. Pryce TM, Wilson RD, Kulski JK (1999) Identification of enterococci by ribotyping with horseradish-peroxidase-labelled 16S rDNA probes. J Microbiol Methods 36:147–155PubMedCrossRefGoogle Scholar
  145. Rich RL, Kreikemeyer B, Owens RT, LaBrenz S, Narayana SV, Weinstock GM, Murray BE, Hook M (1999) Ace is a collagen-binding MSCRAMM from Enterococcus faecalis. J Biol Chem 274:26939–26945PubMedCrossRefGoogle Scholar
  146. Rossi EA, Vendramini RC, Carlos IZ, Pei YC, de Valdez GF (1999) Development of a novel fermented soymilk product with potential probiotic properties. Eur Food Res Technol 209:305–307CrossRefGoogle Scholar
  147. Rovenský J, Švik K, Stančíková M, Ebringer L, Ferenčík M (2002) Treatment of experimental adjuvant arthritis with the combination of methotrexate and lyophilized Enterococcus faecium eniched with organic selenium. Folia Microbiol 47:573–578CrossRefGoogle Scholar
  148. Sannomiya PRA, Craig DB, Clewell A, Suzuki M, Fujino G, Till O, Marasco WA (1990) Characterization of a class of nonformylated Enterococcus faecalis-derived neutrophil chemotactic peptides: the sex pheromones. Proc Natl Acad Sci USA 87:66–70PubMedCrossRefGoogle Scholar
  149. Sarantinopoulos P, Leroy F, Leontopoulou E, Georgalaki MD, Kalantzopoulos G, Tsakalidou E, De VL (2002) Bacteriocin production by Enterococcus faecium FAIR-E 198 in view of its application as adjunct starter in Greek Feta cheese making. Int J Food Microbiol 72:125–136PubMedCrossRefGoogle Scholar
  150. Schleifer KH, Kilpper-Balz R (1984) Transfer of Streptococcus faecalis and Streptococcus faecium to the genus Enterococcus nom. rev. as Enterococcus faecalis comb. nov. and Enterococcus faecium comb. nov. Int J Syst Bacteriol 34:31–34CrossRefGoogle Scholar
  151. Schleifer KH, Kilpper-Bälz R (1987) Molecular and chemotaxonomic approaches to the classification of streptococci, enterococci and lactococci: a review. Syst Appl Microbiol 6:1–19CrossRefGoogle Scholar
  152. Semedo T, Santos MA, Lopes MFS, Marques JJF, Crespo MTB, Tenreiro R (2003) Virulence factors in food, clinical and reference enterococci: a common trait in the genus? Syst Appl Microbiol 26:13–22PubMedCrossRefGoogle Scholar
  153. Shankar N, Baghdayan AS, Gilmore MS (2002) Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417:746–750PubMedCrossRefGoogle Scholar
  154. Shankar N, Lockatell CV, Baghdayan AS, Drachenberg C, Gilmore MS, Johnson DE (2001) Role of Enterococcus faecalis surface protein Esp in the pathogenesis of ascending urinary tract infection. Infect Immun 69:4366–4372PubMedCrossRefGoogle Scholar
  155. Simonetta AC, Moragues de Velasco LG, Frisón LN (1997) Antibacterial activity of enterococci strains against Vibrio cholerae. Lett Appl Microbiol 24:139–143PubMedCrossRefGoogle Scholar
  156. Singh KV, Coque TM, Weinstock GM, Murray BE (1998) In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol Med Microbiol 21:323–331PubMedGoogle Scholar
  157. Son R, Nimita F, Rusul G, Nasreldin E, Samuel L, Nishibuchi M (1999) Isolation and molecular characterization of vancomycin-resistant Enterococcus faecium in Malaysia. Lett Appl Microbiol 29:118–122PubMedCrossRefGoogle Scholar
  158. Su A, Sulavik MC, He P, Mäkinen KK, Mäkinen P, Fiedler S, Wirth R, Clewell DB (1991) Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. Liquefaciens Infect Immun 59:415–420Google Scholar
  159. Süßmuth SD, Muscholl-Silberhorn A, Wirth R, Susa M, Marre R, Rozdzinski E (2002) Aggregation substance promotes adherence, phagocytosis, and intracellular survival of Enterococcus faecalis within human macrophages and suppresses respiratory burst. Infect Immun 68:4900–4906CrossRefGoogle Scholar
  160. Suzzi G, Caruso M, Gardini F, Lombardi A, Vannini L, Guerzoni ME, Andrighetto C, Lanorte MT (2000) A survey of the enterococci isolated from an artisanal Italian goat’s cheese (semicotto caprino). J Appl Microbiol 89:267–274PubMedCrossRefGoogle Scholar
  161. Švec P, Devriese LA, Sedláček I, Baele M, Vancanneyt M, Haesebrouck F, Swings J, Doškář J (2001) Enterococcus haemoperoxidus sp. nov. and Enterococcus moraviensis sp. nov., isolated from water. Int J Syst Evol Microbiol 51:1567–1574PubMedGoogle Scholar
  162. Švec P, Vancanneyt M, Seman M, Snauwaert C, Lefebvre K, Sedlacek I, Swings J (2005) Evaluation of (GTG)5-PCR for identification of Enterococcus spp. FEMS Microbiol Lett 247:59–63PubMedCrossRefGoogle Scholar
  163. Tannock GW, Cook G (2002) Enterococci as members of the intestinal microflora of humans. In: Gilmore MS, Clewell DB,Courvalin P, Dunny GM, Murray BE, Rice LB (eds) The enterococci: pathogenesis, molecular biology, and antibiotic resistance. ASM, Washington, DCGoogle Scholar
  164. Tavaria FK, Malcata FX (1998) Microbiological characterization of Serra da Estrela cheese throughout its Appelation d’Origine Protegée region. J Food Prot 61:601–607PubMedGoogle Scholar
  165. Teng LJ, Hsueh PR, Wang YH, Lin HM, Luh KT, Ho SW (2001) Determination of Enterococcus faecalis groESL Full-Length sequence and application for species identification. J Clin Microbiol 39:3326–3331PubMedCrossRefGoogle Scholar
  166. Teuber M, Meile L, Schwarz F (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie van Leeuwenhoek 76:115–137PubMedCrossRefGoogle Scholar
  167. Titze-de-Almeida R, Willems RJL, Top J, Pereira Rodrigues I, Fonseca Ferreira R, Boelens H, Brandileone MCC, Zanella RC, Soares Felipe MS, van Belkum A (2004) Multilocus variable-number tandemrepeat polymorphism among Brazilian Enterococcus faecalis strains. J Clin Microbiol 42:4879–4881PubMedCrossRefGoogle Scholar
  168. Toledo-Arana A, Valle J, Solano C, Arrizubieta MJ, Cucarella C, Lamata M, Amorena B, Leiva L, Penadés JR, Lasa I (2001) The enterococcal surface protein, esp, is involved in Enterococcus faecalis biofilm formation. Appl Environ Microbiol 67:4538–4545PubMedCrossRefGoogle Scholar
  169. Top J, Schouls LM, Bonten MJ, Willems RJ (2004) Multiple-locus variable-number tandem repeat analysis, a novel typing scheme to study the genetic relatedness and epidemiology of Enterococcus faecium isolates. J Clin Microbiol 42:4503–4511PubMedCrossRefGoogle Scholar
  170. Tornadijo ME, Fresno JM, Bernardo A, Marin Sarmiento R, Carballo J (1995) Microbiological changes throughout the manufacturing and ripening of Spanish goat’s raw milk cheese (Armada variety). Lait 75:551–570CrossRefGoogle Scholar
  171. Torriani S, Dellaglio F, Lombardi A (1998) Microbiological contribution to the study of Monte Veronese cheese. Proceedings of the Symposium “Quality and Microbiology of Traditional and Raw Milk Cheeses”, Dijon, France, pp 239–250Google Scholar
  172. Treitman AN, Yarnold PR, Warren J, Noskin GA (2005) Emerging incidence of Enterococcus faecium among hospital isolates (1993 to 2002). J Clin Microbiol 43:462–463PubMedCrossRefGoogle Scholar
  173. Tyrrell GJ, Bethune RN, Willey B, Low DE (1997) Species identification of enterococci via intergenic ribosomal PCR. J Clin Microbiol 35:1054–1060PubMedGoogle Scholar
  174. Tzanetakis N, Litopoulou-Tzanetaki E (1992) Changes in numbers and kinds of lactic acid bacteria in Feta and Teleme, two Greek cheeses from ewe’s milk. J Dairy Sci 75:1389–1393CrossRefGoogle Scholar
  175. Ulrich A, Muller T (1998) Heterogeneity of plant-associated streptococci as characterized by phenotypic features and restrict tion analysis of PCR-amplified 16S rDNA. J Appl Microbiol 84:293–303PubMedCrossRefGoogle Scholar
  176. Vakulenko SB, Donabedian SM, Voskresenskiy AM, Zervos MJ, Lerner SA, Chow JW (2003) Multiplex PCR for detection of aminoglycoside resistance genes in enterococci. Antimicrob Agents Chemother 47:1423–1426PubMedCrossRefGoogle Scholar
  177. Vancanneyt M, Lombardi A, Andrighetto C, Knijff E, Torriani S, Bjorkroth KJ, Franz CM, Foulquie Moreno MR, Revets H, De Vuyst L, Swings J, Kersters K, Dellaglio F, Holzapfel WH (2002) Intraspecies genomic groups in Enterococcus faecium and their correlation with origin and pathogenicity. Appl Environ Microbiol 68:1381–1390PubMedCrossRefGoogle Scholar
  178. Versalovic J, Schneider M, De Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40Google Scholar
  179. Villani F, Coppola S (1994) Selection of enterococcal strains for water-buffalo Mozzarella cheese manufacture. Annali di Microbiologia ed Enzimologia 44:97–105Google Scholar
  180. Volokhov VD, Chizhikov V, Chumakov K, Rasooly A (2003) Microarray analysis of erythromycin resistance determinants. J Appl Microbiol 95:787–798PubMedCrossRefGoogle Scholar
  181. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB (2004) Nosocomial bloodstream infections in US hospitals: analysis of 24, 179 cases from a prospective nationwide surveillance study. Clin Infect Dis 39:309–317PubMedCrossRefGoogle Scholar
  182. Wunderlich PF, Braun L, Fumagalli I, D´Apuzzo V, Heim F, Karli M, Lodi R, Politta G, Vonbank F, Zdeltner L (1989) Double-blind report on the efficacy of lactic acid producing Enterococcus SF68 in the prevention of antibiotic-associated diarrhoea and in the treatment of acute diarrhoea. J Int Med Res 17:333–338Google Scholar
  183. Zárate V, Belda F, Pérez C, Cardell E (1997) Changes in the microbial flora of Tenerife goat’s milk cheese during ripening. Int Dairy J 7:635–641CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Roman Dušinský
    • 1
  • Anna Belicová
    • 1
  • Libor Ebringer
    • 1
  • Dušan Jurkovič
    • 1
  • Lívia Križková
    • 1
  • Mária Mikulášová
    • 1
  • Juraj Krajčovič
    • 1
    Email author
  1. 1.Institute of Cell Biology, Faculty of Natural SciencesComenius University in BratislavaBratislavaSlovakia

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