Detection of virulence factors in high-level gentamicin-resistant Enterococcus faecalis and Enterococcus faecium isolates from a Tunisian hospital

Canadian Journal of Microbiology

Volumn 53, Issue 3, 2007, Pages 372-379

  Klibi, N ^a   Ben Slama, K ^a   Saenz Y ^b   Masmoudi, A ^c   Zanetti, S ^d   Sechi, L A ^d   Boudabous, A ^a   Torres, C ^b  

^a Campus Universitaire   (Tunisia)

^b UNIVERSITY OF LA RIOJA   (Spain)

^c LA RABTA HOSPITAL   (Tunisia)

^d UNIVERSITY OF SASSARI   (Italy)

Author keywords

Enterococcus faecalis; Enterococcus faecium; High level gentamicin resistance; Tunisia; Virulence factors

Indexed keywords

BIOFILMS; CELLS; GENES; MICROBIOLOGY; PATIENT TREATMENT;

CLINICAL ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECALIS; GELATINASE; HIGH-LEVEL GENTAMICIN RESISTANCE; VIRULENCE FACTORS;

GENETIC ENGINEERING;

CHLORAMPHENICOL; ERYTHROMYCIN; GELATINASE; GENTAMICIN; HEMOLYSIN; KANAMYCIN; PENICILLIN G; STREPTOMYCIN; TETRACYCLINE; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; BACTERIUM; BIOFILM; DETECTION METHOD; ENZYME ACTIVITY; VIRULENCE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CELL ADHESION; CELL STRAIN CACO 2; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENZYME ACTIVITY; GENE SEQUENCE; HEP 2 CELL; HUMAN; HUMAN CELL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; ACE GENE; AGG GENE; CACO 2 CELL LINE; CPD GENE; CYLLLS GENE; ESP GENE; FSRB GENE; GELE GENE; GENOTYPE; HEP 2 CELL LINE; HOSPITAL; PHENOTYPE; TUNISIA;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CACO-2 CELLS; CELL LINE; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; GENTAMICINS; GRAM-POSITIVE BACTERIAL INFECTIONS; HOSPITALS; HUMANS; MICROBIAL SENSITIVITY TESTS; TUNISIA; VIRULENCE; VIRULENCE FACTORS;

AFRICA; NORTH AFRICA; TUNISIA;

ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM;

EID: 34547224055     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W06-136     Document Type: Article

References (51)

1. Archimbaud, C., Shankar, N., Forestier, C., Baghdayan, A., Gilmore, M.S., Charbonne, F., and Joly, B. 2002. In vitro adhesive properties and virulence factors of Enterococcus faecalis strains. Res. Microbiol. 153: 75-80. doi:10.1016/S0923-2508(01)01291-8.
2. Chow, J.W., Thal, L.A., Perri, M.B., Vazquez, J.A., Donabedian, S.M., Clewell, D.B., and Zervos, M.J. 1993. Plasmid-associated hemolysin and aggregation substance production contribute to virulence in experimental enterococcal endocarditis. Antimicrob. Agents Chemother. 37: 2474-2477.
3. Coburn, P.S., and Gilmore, M.S. 2003. The Enterococcus faecalis cytolysin: a novel toxin active against eukaryotic and prokaryotic cells. Cell. Microbiol. 5: 661-669. doi:10.1046/j.1462-5822. 2003.00310.x.
4. Coque, T.M., Patterson, J.E., Steckelberg, J.M., and Murray, B.E. 1995. Incidence of hemolysin, gelatinase and aggregation substance among enterococci isolated from patients with endocarditis and other infections and from faeces of hospitalized and community-based persons. J. Infect. Dis. 171: 1223-1229.
5. Coque, T.M., Willems, R., Canton, R., Del Campo, R., and Baquero, F. 2002. High occurrence of esp among ampicillin-resistant and vancomycin-susceptible Enterococcus faecium clones from hospitalized patients. J. Antimicrob. Chemother. 50: 1035-1038. doi:10.1093/jac/ dkf229.
6. Creti, R., Imperi, M., Bertuccini, L., Fabretti, F., Orefici, G., Di Rosa, R., and Baldassarri, L. 2004. Survey for virulence determinants among Enterococcus faecalis isolated from different sources. J. Med. Microbiol. 53: 13-20. doi:10.1099/jmm.0. 05353-0.
7. De Vuyst, L., Foulquié Moreno, M.R., and Revets, H. 2003. Screening for enterocins and detection of hemolysin and vancomycin resistance in enterococci of different origins. Int. J. Food Microbiol. 84: 299-318. doi:10.1016/S0168-1605(02)00425-7.
8. Di Rosa, R., Creti, R., Venditti, M., D'Amelio, R., Arciola, C.R., Montanaro, L., and Baldassarri, L. 2006. Relationship between biofilm formation, the enterococcal surface protein (Esp) and gelatinase in clinical isolates of Enterococcus faecalis and Enterococcus faecium. FEMS Microbiol. Lett. 256: 145-150. doi:10.1111/j.1574-6968.2006.00112.x.
9. Duprè, I., Zanetti, S., Schito, A.M., Fadda, G., and Sechi, L.A. 2003. Incidence of virulence determinants in clinical Enterococcus faecium and Enterococcus faecalis isolates collected in Sardinia (Italy). J. Med. Microbiol. 52: 491-498. doi:10.1099/jmm. 0.05038-0.
10. Eaton, T.J., and Gasson, M.J. 2001. Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl. Environ. Microbiol. 67: 1628-1635. doi:10.1128/AEM.67.4.1628-1635. 2001.
11. Eisner, H.A., Sobottka, I., Mack, D., Claussen, M., Laufs, R., and Wirth, R. 2000. Virulence factors of Enterococcus faecalis and Enterococcus faecium blood culture isolates. Eur. J. Clin. Microbiol. Infect. Dis. 19: 39-42. doi:10.1007/s100960050007.
12. Ember, J.A., and Hugli, T.E. 1989. Characterization of the human neutrophil response to sex pheromones from Streptococcus faecalis. Am. J. Pathol. 134: 797-805.
13. Ferretti, J.J., Gilmore, K.S., and Courvalin, P. 1986. Nucleotide sequence analysis of the gene specifying the bifunctional 6′- aminoglycoside acetyltransferase 2″-aminoglycoside phosphotransferase enzyme in Streptococcus faecalis and identification and cloning of gene regions specifying the two activities. J. Bacteriol. 167: 631-638.
14. Frazier, W.C. 1926. A method for the detection of changes in gelatine due to bacteria. J. Infect. Dis. 39: 302-309.
15. Galli, D., Lottspeich, F., and Wirth, R. 1990. Sequence analysis of Enterococcus faecalis aggregation substance encoded by the sex pheromone plasmid pAD1. Mol. Microbiol. 4: 895-904. doi:10. 1111/j.1365-2958.1990. tb00662.x.
16. Gutschik, E., Moller, S., and Christensen, N. 1979. Experimental endocarditis in rabbits. 3. Significance of the proteolytic capacity of the infecting strains of Streptococcus faecalis. Acta Pathol. Microbiol. Scand. B, 87: 353-362.
17. Hammerum, A.M., and Jensen, L.B. 2002. Prevalence of esp, encoding the enterococcal surface protein, in Enterococcus faecalis and Enterococcus faecium isolates from hospital patients, poultry, and pigs in Denmark. J. Clin. Microbiol. 40: 4396. doi:10. 1128/JCM.40.11.4396. 2002.
18. Hancock, L.E., and Perego, M. 2004. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J. Bacteriol. 186: 5629-5639. doi:10. 1128/JB.186.17.5629- 5639.2004.
19. Harrington, S.M., Ross, T.L., Gebo, K.A., and Merz, W.G. 2004. Vancomycin resistance, esp and strain relatedness: a 1-year study of enterococcal bacteremia. J. Clin. Microbiol. 42: 5895-5898. doi:10.1128/JCM.42.12. 5895-5898.2004.
20. Jett, B.D., Jensen, H.G., Nordquist, R.E., and Gilmore, M.S. 1992. Contribution of the pAD1-encoded cytolysin to the severity of experimental Enterococcus faecalis endophthalmitis. Infect. Immun. 60: 2445-2452.
21. Johnson, A.P. 1994. The pathogenicity of enterococci. J. Antimicrob. Chemother. 33: 1083-1089.
22. Klibi, N., Gharbi, S., Masmoudi, A., Ben Slama, K., Poeta, P., Zarazaga, M., et al. 2006. Antibiotic resistance and mechanisms implicated in clinical enterococci in a Tunisian Hospital. J. Chemother. 18: 20-26.
23. Kreft, B., Marre, R., Schramm, U., and Wirth, R. 1992. Aggregation substance of Enterococcus faecalis mediates adhesion to cultured renal tubular cells. Infect. Immun. 60: 25-30.
24. Kristich, C.J., Li, Y.H., Cvitkovitch, D.G., and Dunny, G.M. 2004. Esp-Independent biofilm formation by Enterococcus faecalis. J. Bacteriol. 186: 154-163. doi: 10.1128/JB.186.1.154-163.2004.
25. Mannu, L., Paba, A., Daga, E., Comunian, R., Zanetti, S., Dupre, 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. Int. J. Food Microbiol. 88: 291-304. doi:10.1016/S0168-1605(03) 00191-0.
26. Mohamed, J.A., Huang, W., Nallapareddy, S.R., Teng, F., and Murray, B.E. 2004. Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect. Immun. 72: 3658-3663. doi:10. 1128/IAI.72.6.3658-3663.2004.
27. Mundy, L.M., Sahm, D.F., and Gilmore, M. 2000. Relationships between enterococcal virulence and antimicrobial resistance. Clin. Microbiol. Rev. 13: 513-522. doi:10.1128/CMR.13.4.513-522.2000.
28. Murray, B.E. 1998. Diversity among multidrug-resistant enterococci. Emerg. Infect. Dis. 4: 37-47.
29. Nakayama, J., Kariyama, R., and Kumon, H. 2002. Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl. Environ. Microbiol. 68: 3152-3155. doi:10.1128/AEM.68.6.3152-3155.2002.
30. Nallapareddy, S.R., Qin, X., Weinstock, G.M., Höök, M., and Murray, B.E. 2000a. Enterococcus faecalis adhesin, Ace, mediates attachment to extracellular matrix proteins collagen type IV and laminin as well as collagen type I. Infect. Immun. 68: 5218-5224. doi:10.1128/IAI.68.9. 5218-5224.2000.
31. Nallapareddy, S.R., Singh, K.V., Duh, R.W., Weinstock, G.M., and Murray, B.E. 2000b. Diversity of ace, a gene encoding a microbial surface component recognizing adhesive matrix molecules, from different strains of Enterococcus faecalis and evidence for production of Ace during human infections. Infect. Immun. 68: 5210-5217. doi:10.1128/IAI.68.9.5210-5217. 2000.
32. Nallapareddy, S.R., Duh, R.W., Singh, K.V., and Murray, B.E. 2002. Molecular typing of selected Enterococcus faecalis isolates: pilot study using multilocus sequence typing and pulsed-field-gel electrophoresis. J. Clin. Microbiol. 40: 868-876. doi:10.1128/JCM.40.3.868-876.2002.
33. Olmsted, S.B., Dunny, G.M., Erlandsen, S.L., and Wells, C.L. 1994. A plasmid-encoded surface protein on Enterococcus faecalis augments its internalization by cultured intestinal epithelial cells. J. Infect. Dis. 170: 1549-1556.
34. Poeta, P., Costa, D., Sáenz, Y., Klibi, N., Ruiz-Larrea, F., Rodrigues, J., and Torres, C. 2005. Characterization of antibiotic resistance genes and virulence factors in faecal enterococci of wild animals in Portugal. J. Vet. Med. B, 52: 396-402. doi:10.1111/j.1439-0450.2005.00881.x.
35. Poeta, P., Costa, D., Klibi, N., Rodrigues, J., and Torres, C. 2006. Phenotypic and genotypic study of gelatinase and beta-haemolysis activities in faecal enterococci of poultry in Portugal. J. Vet. Med. B, 53: 203-208. doi:10.1111/j.1439-0450.2006.00941.x.
36. Ramadhan, A.A., and Hegedus, E. 2005. Biofilm formation and esp gene carriage in enterococci. J. Clin. Pathol. 58: 685-686. doi:10.1136/jcp.2004.024109.
37. Rich, R.L., Kreikemeyer, B., Owens, R.T., LaBrenz, S., Narayana, S.V., Weinstock, G.M., Murray, B.E., and Hook, M. 1999. Ace is a collagen-binding MSCRAMM from Enterococcus faecalis. J. Biol. Chem. 274: 26939-26945. doi:10.1074/jbc.274.38.26939.
38. Roberts, J.C., Singh, K.V., Okhuysen, P.C., and Murray, B.E. 2004. Molecular epidemiology of the fsr locus and gelatinase production among different subsets of Enterococcus faecalis isolates. J. Clin. Microbiol. 42: 2317-2320. doi:10.1128/JCM.42.5.2317-2320.2004.
39. Rozdzinski, E., Marre, R., Susa, M., Wirth, R., and Muscholl-Silberhorn, A. 2001. Aggregation substance-mediated adherence of Enterococcus faecalis to immobilized extracellular matrix proteins. Microb. Pathog. 30: 211-220. doi:10.1006/mpat.2000.0429.
40. Semedo, T., Almeida Santos, M., Silva Lopes, M.F., Martins, P., Figueiredo Marques, J.J., Tenreiro, R., and Barreto Crespo, M.T. 2003. Comparative study using type strains and clinical and food isolates to examine hemolytic activity and occurence of the cyl operon in enterococci. J. Clin. Microbiol. 41: 2569-2576. doi:10.1128/JCM.41.6.2569-2576.2003.
41. Shankar, N., Lockatell, C.V., Baghdayan, A.S., Drachenberg, C., Gilmore, M.S., and Johnson, D.E. 2001. Role of Enterococcus faecalis surface protein Esp in the pathogenesis of ascending urinary tract infection. Infect. Immun. 69: 4366-4372. doi:10.1128/IAI.69.7.4366-4372.2001.
42. Shankar, V., Baghdayan, A.S., Huycke, M.M., Lindahl, G., and Gilmore, M.S. 1999. Infection-derived Enterococcus faecalis strains are enriched in esp, a gene encoding a novel surface protein. Infect. Immun. 67: 193-200.
43. Su, Y.A., Sulavik, M.C., He, P., Makinen, K.K., Makinen, P.L., Fiedler, S., Wirth, R., and Clewell, D.B. 1991. Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. liquefaciens. Infect. Immun. 59: 415-420.
44. Toledo-Arana, A., Valle, J., Solano, C., Arrizubieta, M.J., Cucarella, C., Lamata, M., et al. 2001. The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol. 67: 4538-4545. doi:10.1128/AEM.67.10.4538-4545.2001.
45. Vergis, E.N., Shankar, N., Chow, J.W., Hayden M.K., Snydman, D.R., Zervos, M.J., et al. 2002. Association between the presence of enterococcal virulence factors gelatinase, hemolysin, and enterococcal surface protein and mortality among patients with bacteremia due to Enterococcus faecalis. Clin. Infect. Dis. 35: 570-575. doi:10.1086/341977.
46. Waar, K., Muscholl-Silberhorn, A.B., Willems, R.J., Slooff, M.J., Harmsen, H.J., and Degener, J.E. 2002. Genogrouping and incidence of virulence factors of Enterococcus faecalis in liver transplant patients differ from blood culture and fecal isolates. J. Infect. Dis. 185: 1121-1127. doi:10.1086/339682.
47. Willems, R.J., Homan, W., Top, J., van Santen-Verheuvel, M., Tribe, D, Manzioros, X., et al. 2001. Variant esp gene as a marker of a distinct genetic lineage of vancomycin resistant Enterococcus faecium spreading in hospitals. Lancet, 357: 853-855. doi:10.1016/S0140-6736(00)04205-7.
48. Wirth, R. 1994. The sex pheromone system of Enterococcus faecalis More than just a plasmid-collection mechanism? Eur. J. Biochem. 222: 235-246. doi:10.1111/j.1432-1033.1994.tb18862.x.
49. Woodford, N., Soltani, M., and Hardy, K.J. 2001. Frequency of esp in Enterococcus faecium isolates. Lancet, 358: 584. doi:10.1016/S0140-6736(01)05726-9.
50. Zanetti, S., Sechi, L., Angioi, A., Perazzona, B., and Fadda, G. 1992. Entry of pyelonephritogenic Escherichia coli into Hep-2 cells due to actin polymerization. Microbiologica, 15: 117-123.
51. Zeng, J., Teng, F., and Murray, B.E. 2005. Gelatinase is important of translocation of Enterococcus faecalis across polarized human enterocyte-like T84 cells. Infect. Immun. 73: 1606-1612. doi:10.1128/IAI.73.3.1606-1612.2005.