Genetic diversity and safety aspects of enterococci from slightly fermented sausages

Journal of Applied Microbiology

Volumn 98, Issue 5, 2005, Pages 1177-1190

  Martin, B ^a   Garriga, M ^a   Hugas, M ^b   Aymerich, Teresa ^a  

^a IRTA   (Spain)

^b EUROPEAN FOOD SAFETY AUTHORITY   (Italy)

Author keywords

Antibiotic resistance; Enterococci; Fermented sausages; RAPD PCR; Virulence genes

Indexed keywords

ANTIBIOTICS; BACILLI; BIODIVERSITY; HEALTH RISKS; MEATS; POLYMERASE CHAIN REACTION; RNA; SAFETY ENGINEERING;

ANTIBIOTICS RESISTANCE; ENTEROCOCCUS; FERMENTED SAUSAGES; GENETICS DIVERSITIES; RANDOMLY AMPLIFIED POLYMORPHIC DNA; RANDOMLY AMPLIFIED POLYMORPHIC DNA-PCR; SAFETY ASPECTS; SPECIES SPECIFICS; STRAIN LEVELS; VIRULENCE GENE;

GENES;

AMPICILLIN; ANTIBIOTIC AGENT; CHLORAMPHENICOL; CIPROFLOXACIN; DALFOPRISTIN PLUS QUINUPRISTIN; ERYTHROMYCIN; GENTAMICIN; GLYCOPEPTIDE; LINEZOLID; NITROFURANTOIN; PENICILLIN G; RIFAMPICIN; RNA 16S; TEICOPLANIN; TETRACYCLINE; VANCOMYCIN; VIRULENCE FACTOR;

FOOD SAFETY; GENETIC VARIATION; MICROBIOLOGY;

AGG GENE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BACTERIUM ISOLATION; CONTROLLED STUDY; EFAAFM GENE; EFAAFS GENE; ENTEROCOCCUS; ENTEROCOCCUS CASSELIFLAVUS; ENTEROCOCCUS DURANS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS FLAVESCENS; ENTEROCOCCUS GALLINARUM; ENTEROCOCCUS HIRAE; ESP GENE; FERMENTATION; FOOD QUALITY; FOOD SAFETY; GELE GENE; GENE; GENETIC VARIABILITY; GENOTYPE; HEALTH HAZARD; MEAT; MICROBIAL DIVERSITY; MOLECULAR TYPING; MULTIDRUG RESISTANCE; NONHUMAN; POLYMERASE CHAIN REACTION; RANDOM AMPLIFIED POLYMORPHIC DNA; RNA SEQUENCE; SODA GENE; SPECIES DIFFERENCE; VANA GENE; VANC1 GENE; VANC2 GENE; VANC3 GENE; VANCOMYCIN RESISTANT ENTEROCOCCUS;

ENTEROCOCCUS CASSELIFLAVUS; ENTEROCOCCUS DURANS; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENTEROCOCCUS GALLINARUM; ENTEROCOCCUS HIRAE;

EID: 17644396612     PISSN: 13645072     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2005.02555.x     Document Type: Article

References (63)

1. Adams, M.R. (1999) Safety of industrial lactic acid bacteria. Journal of Biotechnology 68, 171-178.
2. Angeletti, S., Lorino, G., Gherardi, G., Battistoni, F., De Cesaris, M. and Dicuonzo, G.R. (2001) Routine molecular identification of enterococci by gene-specific PCR and 16S ribosomal DNA sequencing. Journal of Clinical Microbiology 39, 794-797.
3. Antonishyn, N.A., McDonald, R.R., Chan, E.L., Horsman, G., Woodmansee, C.E., Falk, P.C. and Mayhall, G.G. (2000) Evaluation of fluorescence-based amplified fragment length polymorphism analysis for molecular typing in hospital epidemiology: comparison with pulsed-field gel electrophoresis for typing strains of vancomycin-resistant Enterococcus faecium. Journal of Clinical Microbiology 38, 4058-4065.
4. Arthur, M., Reynolds, P. and Courvalin, P (1996) Glycopeptide resistance in enterococci. Trends in Microbiology 4, 401-407.
5. Aymerich, M.T., Garriga, M., Ylla, J., Valuer, J., Monfort, J.M. and Hugas, M. (2000) Application of enterocins as biopreservatives against Listeria innocua in meat products. Journal of Food Protection 63, 721-726.
6. Aymerich, M.T., Martín, B., Garriga, M. and Hugas, M. (2003) Microbial quality and direct PCR identification of lactic acid bacteria and nonpathogenic staphylococci from artisanal low-acid sausages. Applied and Environmental Microbiology 69, 4583-4594.
7. Baumgartner, A., Kueffer, M. and Rohner, P. (2001) Occurrence and antibiotic resistance of enterococci in various ready-to-eat foods. Archiv fur Lebensmittel Hygiene 52, 16-19.
8. CDC NNIS System (1998) National Nosocomial Infections Surveillance (NNIS) report, data summary from October 1986-April 1998, issued June 1998. American Journal of Infection Control 26, 522-533.
9. Centeno, J.A., Menéndez, S. and Rodríguez-Otero, J.L. (1996) Main microbial flora present as natural starters in Cebreiro raw cow's-milk cheese (Northwest Spain). International Journal of Food Microbiology 33, 307-313.
10. Charteris, W.P., Kelly, P.M., Morelli, L. and Collins, J.K. (1998) Antibiotic susceptibility of potentially probiotic Lactobacillus species. Journal of Food Protection 61, 1636-1643.
11. Cheng, S., McCleskey, F.K., Gress, M.J., Petroziello, J.M., Liu, R., Namdari, H., Beninga, K., Salmen, A. et al. (1997) A PCR assay for identification of Enterococcus faecium. Journal of Clinical Microbiology 35, 1248-1250.
12. Clewell, D.B. (1990) Movable genetic elements and antibiotic resistance in enterococci. European Journal of Clinical Microbiology and Infectious Diseases 9, 90-102.
13. Cocconcelli, P.S., Porro, D., Galandini, S. and Senini, L. (1995) Development of RAPD protocol for typing of strains of lactic acid bacteria and enterococci. Letters in Applied Microbiology 21, 376-379.
14. Cocconcelli, P.S., Cattivelli, D. and Gazzola, S. (2003) Gene transfer of vancomycin and tetracycline resistances among Enterococcus faecalis during cheese and sausage fermentations. International Journal of Food Microbiology 88, 315-323.
15. Collins, M.D., Farrow, J.A.E. and Jones, D. (1986) Enterococcus mundtii sp. Nov. International Journal of Systematic Bacteriology 36, 8-12.
16. Coppola, S., Parente, E., Dumontet, S. and La Peccerella, A. (1988) The microflora of natural whey cultures utilized as starters in the manufacture of Mozzarella cheese from water-buffalo milk. Lait 68, 295-310.
17. Descheemaeker, P., Lammens, C., Pot, B., Vandamme, P. and 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. International Journal of Systematic Bacteriology 47, 555-561.
18. Devriese, L.A. and Pot, B. (1995) The genus Enterococcus. In The Lactic Acid Bacteria ed. Wood, B.J.B. and Holzapfel, W.H. pp. 328-367. London: Blackie Academic.
19. Devriese, L.A., Van De Kerckhove, A., Kilpper-Bälz, R. and Schleifer, K.H. (1987) Characterization and identification of Enterococcus species isolated from animals. International Journal of Systematic Bacteriology 37, 257-259.
20. Devrkse, L.A., Pot, B., Van Damme, L., Kersters, K. and Haesebrouck, F. (1995) Identification of Enterococcus species isolated from foods of animal origin. International Journal of Food Microbiology 26, 187-197.
21. Devriese, L.A., Pot, B., Kersters, K., Lauwers, S. and Haesebrouck, F. (1996) Acidification of methyl-alpha-D-glucopyranoside: a useful test to differentiate Enterococcus casseliflavus and Enterococcus gallinarum from Enterococcus faecium species group and from Enterococcus faecalis. Journal of Clinical Microbiology 34, 2607-2608.
22. Devriese, L.A., Vancanneyt, M., Descheemaeker, P., Baele, M., Van Landuyt, H.W., Gordts, B., Butaye, P., Swings, J. et al. (2002) Differentiation and identification of Enterococcus durans, E. hirae and E. villorum. Journal of Applied Microbiology 92, 821-827.
23. Domig, K.J., Mayer, H.K. and Kneifel, W. (2003) Methods used for the isolation, enumeration, characterisation and identification of Enterococcus spp. 2. Pheno- and genotypic criteria. International Journal of Food Microbiology 88, 165-188.
24. Dunny, G.M. (1990) Genetic functions and cell-cell interactions in the pheromone-inducible plasmid transfer system of Enterococcus faecalis. Molecular Microbiology 4, 689-696.
25. Dunny, G.M., Leonard, B.A. and Hedberg, P.J. (1995) Pheromone inducible conjugation in Enterococcus faecalis: interbacterial and host-parasite chemical communication. Journal of Bacteriology 177, 871-876.
26. Dupré, I., Zanetti, S., Schito, A.M., Fadda, S. and Sechi, L.A. (2003) Incidence of virulence determinants in clinical Enterococcus faecium and Enterococcus faecalis isolates collected in Sardinia (Italy). Journal of Medical Microbiology 52, 491-498.
27. Dutka-Malen, S., Evers, S. and Courvalin, P. (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. Journal of Clinical Microbiology 33, 24-27.
28. Eaton, T.J. and Gasson, M.J. (2001) Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Applied and Environmental Microbiology 67, 1628-1635.
29. 2 environments. International Journal of Food Microbiology 32, 133-144.
30. Franz, C.M., Holzapfel, W. and Stiles, M.E. (1999) Enterococci at the crossroads of food safety?. International Journal of Food Microbiology 47, 1-24.
31. Franz, C.M., Muscholl-Silberhorn, A.B., Yousif, N.M., Vancanneyt, M., Swings, J. and Holzapfel, W.H. (2001) Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Applied and Environmental Microbiology 67, 4385-4389.
32. Giraffa, G. (2002) Enterococci from foods. FEMS Microbiology Reviews 26, 163-171.
33. Giraffa, G., Olivari, A.M. and Neviani, E. (2000) Isolation of vancomycin-resistant Enterococcus faecium from Italian cheeses. Food Microbiology 39, 2354-2355.
34. Haas, W. and Gilmore, M.S. (1999) Molecular nature of a novel bacterial toxin: the cytolysin of Enterococcus faecalis. Medical Microbiology and Immunology 187, 183-190.
35. Heatorf, M.P., Discotto, L.F., Pucci, M.J. and Handwerger, S. (1996) Mobilization of vancomycin resistance by transposon-mediated fusion of a VanA plasmid with an Enterococcus faecium sex pheromone-response plasmid. Gene 171, 9-17.
36. Jett, B., Huycke, M.M. and Gilmore, M.S. (1994) Virulence of enterococci. Clinical Microbiology Reviews 7, 462-478.
37. Ke, D., Picard, F.J., Martineau, F., Ménard, C., Roy, P.H., Ouellette, M. and Bergeron, M.G. (1999) Development of a PCR assay for rapid detection of enterococci. Journal of Clinical Microbiology 37, 3497-3503.
38. Klein, G. (2003) Taxonomy, ecology and antibiotic resistance of enterococci from food and the gastro-intestinal tract. International Journal of Food Microbiology 88, 123-131.
39. Klein, G., Pack, A. and Reuter, G. (1998) Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany. Applied and Environmental Microbiology 64, 1825-1830.
40. Knudtson, L.M. and Hartman, P.A. (1993) Antibiotic resistance among enterococcal isolates from environmental and clinical sources. Journal of Food Protection 56, 486-492.
41. Leclercq, R. (1997) Enterococci acquire new kinds of resistance. Clinical Infectious Diseases 24, S80-S84.
42. Leclercq, R., Derlot, M., Weber, J., Duval, J. and Courvalin, P. (1989) Transferable vancomycin and teicoplanin resistance in Enterococcus faecium. Antimicrobial Agents and Chemotherapy 33, 10-15.
43. Lowe, A.M., Lambert, P.A. and Smith, A.W. (1995) Cloning of an Enterococcus faecalis endocarditis antigen: homologyb with adhesins from some oral streptococci. Infection and Immunity 63, 703-706.
44. Mannu, L., Paba, A., Daga, E., Comunian, R., Zanetti, S., Duprè, I. and Sechi, L.A. (2003) Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin. International Journal of Food Microbiology 88, 291-304.
45. Morrison, D., Woodford, N. and Cookson, B. (1997) Enterococci as emerging pathogens of humans. Journal of Applied Microbiology. Symposium Supplement 83, 89S-99S.
46. Mundy, L.M., Sahm, D.F. and Gilmore, M.S. (2000) Relationship between enterococcal virulence and antimicrobial resistance. Clinical Microbiology Reviews 13, 513-522.
47. Murray, B.E. (1990) The life and times of the Enterococcus. Clinical Microbiology Reviews 3, 46-65.
48. NCCLS (2002) Performance Standards for Antimicrobial Susceptibility Testing; Twelfth Informational Supplement. NCCLS document M100-S12.940. Wayne, PA: National Committee for Clinical Laboratory Standards.
49. Niemi, R.M., Niemelä, S.I., Bamfort, D.H., Hantula, J., Hyvärinen, T., Forsten, T. and Raateland, A. (1993) Presumptive fecal streptococci in environmental samples characterized by one-dimensional sodium dodecyl sulphate-polyacrylamide gel electrophoresis. Applied and Environmental Microbiology 59, 2190-2196.
50. Noble, W.C., Virani, Z. and Cree, R.G. (1992) Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC 12201 to Staphylococcus aureus. FEMS Microbiology Letters 72, 195-198.
51. Peters, J., Mac, K., Wichmann-Schauer, H., Klein, G. and Ellerbroek, L. (2003) Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany. International Journal of Food Microbiology 88, 311-314.
52. Poyart, C., Quesnes, G. and Trieu-Cuot, P. (2000) Sequencing the gene encoding manganese-dependent superoxide dismutase for rapid species identification of enterococci. Journal of Clinical Microbiology 38, 415-418.
53. Quednau, M., Ahrné, S., Petersson, A.C. and Molin, G. (1998) Antibiotic-resistant strains of Enterococcus isolated from Swedish and Danish retailed chicken and pork. Journal of Applied Microbiology 84, 1163-1170.
54. Reuter, G. (1995) Culture media for enterococci and group D-streptococci. In Culture Media for Food Microbiology Progress in Industrial Microbiology ed. Corry, J.E.L., Curtis, G.D.W. and Baird, R.M. pp. 51-61. Philadelphia, PA: Elsevier Health Sciences.
55. Robredo, B., Singh, K.V., Baquero, F., Murray, B.E. and Torres, C. (2000) Vancomycin-resistant enterococci isolated from animals and food. International Journal of Food Microbiology 54, 197-204.
56. Semedo, T., Almeida, M., Silva Lopes, M.F., Figueiredo Marques, J.J., Barreto Crespo, M.T. and Tenreiro, R. (2003) Virulence factors in food, clinical and reference enterococci: a common trait in the genus? Systematic and Applied Microbiology 26, 13-22.
57. Shankar, V., Baghdayan, A.S., Huycke, M.M., Kindahl, G. and Gilmore, M.S. (1999) Infection-derived Enterococcus faecalis strains are enriched in esp, a gene encoding a novel surface protein. Infection and Immunity 67, 193-200.
58. Singh, K.V., Coque, T.M., Weinstock, G.M. and Murray, B.E. (1998) In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunology and Medical Microbiology 21, 323-331.
59. Swenson, J.M., Bertha, C.H. and Thornsberry, C. (1989) Problems with the disk diffusion test for detection of vancomycin resistance in enterococci. Journal of Clinical Microbiology 27, 2140-2142.
60. Temmerman, R., Pot, B., Huys, G. and Swings, J. (2003) Identification and antibiotic susceptibility of bacterial isolates from probiotic products. International Journal of Food Microbiology 81, 1-10.
61. Teuber, M., Meile, L. and Schwarz, F. (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie van Leeuwenhoek 76, 115-137.
62. Vancanneyt, M., Lombardi, A., Andrighetto, C., Knijff, E., Torriani, S., Björkroth, K.J., Franz, C.M.A.P., Moreno, M.R.F. et al (2002) Intraspecies genomic groups in Enterococcus faecium and their correlation with origin and pathogenicity. Applied and Environmental Microbiology 68, 1381-1391.
63. Wegener, H.C., Aarestrup, P.M., Jensen, L.B., Hammerum, A.M. and Bager, F. (1999) Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic antimicrobial drugs in Europe. Emerging Infectious Diseases 5, 329-335.