1887

Abstract

Enterococci are an important global cause of nosocomial infections, being increasingly associated with urinary tract infections, endocarditis, intra-abdominal and pelvic infections, catheter-related infections, surgical wound infections, and central nervous system infections. The two most common enterococci species are and . Both are capable of producing biofilms, which consist of a population of cells attached irreversibly on various biotic and abiotic surfaces, encased in a hydrated matrix of exopolymeric substances. Many environmental and genetic factors are associated or have been proposed to be associated with the production of biofilm. This review discusses recent advances in knowledge about the biology and genetics of biofilm formation and the role of biofilms in enterococci pathogenesis.

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2007-12-01
2019-10-15
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References

  1. Baldassarri, L., Cecchini, R., Bertuccini, L., Ammendolia, M. G., Iosi, F., Arciola, C. R., Montanaro, L., Di Rosa, R., Gherardi, G. & other authors ( 2001; ). Enterococcus spp. produces slime and survives in rat peritoneal macrophages. Med Microbiol Immunol 190, 113–120.
    [Google Scholar]
  2. Baldassarri, L., Bertuccini, L., Ammendolia, M. G., Cocconcelli, P., Arciola, C. R., Montanaro, L., Creti, R. & Orefici, G. ( 2004; ). Receptor-mediated endocytosis of biofilm-forming Enterococcus faecalis by rat peritoneal macrophages. Indian J Med Res 119 (Suppl.), 131–135.
    [Google Scholar]
  3. Baldassarri, L., Creti, R., Recchia, S., Pataracchia, M., Alfarone, G., Orefici, G., Campoccia, D., Montanaro, L. & Arciola, C. R. ( 2006; ). Virulence factors in enterococcal infections of orthopedic devices. Int J Artif Organs 29, 402–406.
    [Google Scholar]
  4. Bourgogne, A., Singh, K. V., Fox, K. A., Plughoeft, K. J., Murray, B. E. & Garsin, D. A. ( 2007; ). EbpR is important for biofilm formation by activating expression of the endocarditis and biofilm-associated pilus operon (ebpABC) of Enterococcus faecalis OG1RF. J Bacteriol 189, 6490–6493.[CrossRef]
    [Google Scholar]
  5. Breton, Y. L., Maze, A., Hartke, A., Lemarinier, S., Auffray, Y. & Rince, A. ( 2002; ). Isolation and characterization of bile salts-sensitive mutants of Enterococcus faecalis. Curr Microbiol 45, 434–439.[CrossRef]
    [Google Scholar]
  6. Carniol, K. & Gilmore, M. S. ( 2004; ). Signal transduction, quorum-sensing and extracellular protease activity in Enterococcus faecalis biofilm formation. J Bacteriol 186, 8161–8163.[CrossRef]
    [Google Scholar]
  7. Costerton, J. W. ( 2001; ). Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol 9, 50–52.[CrossRef]
    [Google Scholar]
  8. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. ( 1999; ). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322.[CrossRef]
    [Google Scholar]
  9. Creti, R., Koch, S., Fabretti, F., Baldassarri, L. & Huebner, J. ( 2006; ). Enterococcal colonization of the gastro-intestinal tract: role of biofilm and environmental oligosaccharides. BMC Microbiol 6, 60 [CrossRef]
    [Google Scholar]
  10. Dautle, M. P., Wilkinson, T. R. & Gauderer, M. W. ( 2003; ). Isolation and identification of biofilm microorganisms from silicone gastrostomy devices. J Pediatr Surg 38, 216–220.[CrossRef]
    [Google Scholar]
  11. Di Rosa, R., Creti, R., Venditti, M., D'Amelio, R., Arciola, C. R., Montanaro, L. & 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.[CrossRef]
    [Google Scholar]
  12. Distel, J. W., Hatton, J. F. & Gillespie, M. J. ( 2002; ). Biofilm formation in medicated root canals. J Endod 28, 689–693.[CrossRef]
    [Google Scholar]
  13. Dowidar, N., Moesgaard, F. & Matzen, P. ( 1991; ). Clogging and other complications of endoscopic biliary endoprostheses. Scand J Gastroenterol 26, 1132–1136.[CrossRef]
    [Google Scholar]
  14. Dupre, I., Zanetti, S., Schito, A. M., Fadda, G. & 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.[CrossRef]
    [Google Scholar]
  15. Dworniczek, E., Wojciech, L., Sobieszczanska, B. & Seniuk, A. ( 2005; ). Virulence of Enterococcus isolates collected in Lower Silesia (Poland). Scand J Infect Dis 37, 630–636.[CrossRef]
    [Google Scholar]
  16. Eaton, T. J. & Gasson, M. J. ( 2002; ). A variant enterococcal surface protein Esp(fm) in Enterococcus faecium; distribution among food, commensal, medical and environmental isolates. FEMS Microbiol Lett 216, 269–275.[CrossRef]
    [Google Scholar]
  17. Engelbert, M., Mylonakis, E., Ausubel, F. M., Calderwood, S. B. & Gilmore, M. S. ( 2004; ). Contribution of gelatinase, serine protease, and fsr to the pathogenesis of Enterococcus faecalis endophthalmitis. Infect Immun 72, 3628–3633.[CrossRef]
    [Google Scholar]
  18. Fabretti, F., Theilacker, C., Baldassarri, L., Kaczynski, Z., Kropec, A., Holst, O. & Huebner, J. ( 2006; ). Alanine esters of enterococcal lipoteichoic acid play a role in biofilm formation and resistance to antimicrobial peptides. Infect Immun 74, 4164–4171.[CrossRef]
    [Google Scholar]
  19. Gallardo-Moreno, A. M., Gonzalez-Martin, M. L., Perez-Giraldo, C., Bruque, J. M. & Gomez-Garcia, A. C. ( 2002; ). Serum as a factor influencing adhesion of Enterococcus faecalis to glass and silicone. Appl Environ Microbiol 68, 5784–5787.[CrossRef]
    [Google Scholar]
  20. Hancock, L. E. & Perego, M. ( 2004; ). The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J Bacteriol 186, 5629–5639.[CrossRef]
    [Google Scholar]
  21. Hufnagel, M., Koch, S., Creti, R., Baldassarri, L. & Huebner, J. ( 2004; ). A putative sugar-binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. J Infect Dis 189, 420–430.[CrossRef]
    [Google Scholar]
  22. Jett, B. D., Huycke, M. M. & Gilmore, M. S. ( 1994; ). Virulence of enterococci. Clin Microbiol Rev 7, 462–478.
    [Google Scholar]
  23. Jones, M. E., Draghi, D. C., Thornsberry, C., Karlowsky, J. A., Sahm, D. F. & Wenzel, R. P. ( 2004; ). Emerging resistance among bacterial pathogens in the intensive care unit – a European and North American Surveillance study (2000–2002). Ann Clin Microbiol Antimicrob 3, 14 [CrossRef]
    [Google Scholar]
  24. Joyanes, P., Pascual, A., Martinez-Martinez, L., Hevia, A. & Perea, E. J. ( 1999; ). In vitro adherence of Enterococcus faecalis and Enterococcus faecium to plastic biomaterials. Clin Microbiol Infect 5, 382–386.[CrossRef]
    [Google Scholar]
  25. Joyanes, P., Pascual, A., Martinez-Martinez, L., Hevia, A. & Perea, E. J. ( 2000; ). In vitro adherence of Enterococcus faecalis and Enterococcus faecium to urinary catheters. Eur J Clin Microbiol Infect Dis 19, 124–127.[CrossRef]
    [Google Scholar]
  26. Keane, P. F., Bonner, M. C., Johnston, S. R., Zafar, A. & Gorman, S. P. ( 1994; ). Characterization of biofilm and encrustation on ureteric stents in vivo. Br J Urol 73, 687–691.[CrossRef]
    [Google Scholar]
  27. Kobayakawa, S., Jett, B. D. & Gilmore, M. S. ( 2005; ). Biofilm formation by Enterococcus faecalis on intraocular lens material. Curr Eye Res 30, 741–745.[CrossRef]
    [Google Scholar]
  28. Kristich, C. J., Li, Y. H., Cvitkovitch, D. G. & Dunny, G. M. ( 2004; ). Esp-independent biofilm formation by Enterococcus faecalis. J Bacteriol 186, 154–163.[CrossRef]
    [Google Scholar]
  29. Lewis, K. ( 2001; ). Riddle of biofilm resistance. Antimicrob Agents Chemother 45, 999–1007.[CrossRef]
    [Google Scholar]
  30. Miller, M. B. & Bassler, B. L. ( 2001; ). Quorum sensing in bacteria. Annu Rev Microbiol 55, 165–199.[CrossRef]
    [Google Scholar]
  31. Mohamed, J. A. & Murray, B. E. ( 2005; ). Lack of correlation of gelatinase production and biofilm formation in a large collection of Enterococcus faecalis isolates. J Clin Microbiol 43, 5405–5407.[CrossRef]
    [Google Scholar]
  32. Mohamed, J. A. & Murray, B. E. ( 2006; ). Influence of the fsr locus on biofilm formation by Enterococcus faecalis lacking gelE. J Med Microbiol 55, 1747–1750.[CrossRef]
    [Google Scholar]
  33. Mohamed, J. A., Singh, K. V., Huang, W., Teng, F. & Murray, B. E. ( 2003; ). Influence of clinical origin and of various genes on biofilm formation by Enterococcus faecalis. In Program Abstracts of the 43rd Annual Interscience Conference on Antimicrobial Agents and Chemotherapy, abstract B-821, p. 52. Washington, DC: American Society for Microbiology.
  34. Mohamed, J. A., Huang, W., Nallapareddy, S. R., Teng, F. & 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.[CrossRef]
    [Google Scholar]
  35. Mohamed, J. A., Teng, F., Nallapareddy, S. R. & Murray, B. E. ( 2006; ). Pleiotrophic effects of 2 Enterococcus faecalis sagA-like genes, salA and salB, which encode proteins that are antigenic during human infection, on biofilm formation and binding to collagen type I and fibronectin. J Infect Dis 193, 231–240.[CrossRef]
    [Google Scholar]
  36. Molander, A., Reit, C., Dahlen, G. & Kvist, T. ( 1998; ). Microbiological status of root-filled teeth with apical periodontitis. Int Endod J 31, 1–7.[CrossRef]
    [Google Scholar]
  37. Murray, B. E. & Weinstock, G. M. ( 1999; ). Enterococci: new aspects of an old organism. Proc Assoc Am Physicians 111, 328–334.[CrossRef]
    [Google Scholar]
  38. Nakayama, J., Cao, Y., Horii, T., Sakuda, S., Akkermans, A. D., de Vos, W. M. & Nagasawa, H. ( 2001; ). Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol Microbiol 41, 145–154.[CrossRef]
    [Google Scholar]
  39. Nallapareddy, S. R., Singh, K. V., Sillanpaa, J., Garsin, D. A., Hook, M., Erlandsen, S. L. & Murray, B. E. ( 2006; ). Endocarditis and biofilm-associated pili of Enterococcus faecalis. J Clin Invest 116, 2799–2807.[CrossRef]
    [Google Scholar]
  40. O'Toole, G., Kaplan, H. B. & Kolter, R. ( 2000; ). Biofilm formation as microbial development. Annu Rev Microbiol 54, 49–79.[CrossRef]
    [Google Scholar]
  41. Peciuliene, V., Balciuniene, I., Eriksen, H. M. & Haapasalo, M. ( 2000; ). Isolation of Enterococcus faecalis in previously root-filled canals in a Lithuanian population. J Endod 26, 593–595.[CrossRef]
    [Google Scholar]
  42. Pillai, S. K., Sakoulas, G., Eliopoulos, G. M., Moellering, R. C., Jr, Murray, B. E. & Inouye, R. T. ( 2004; ). Effects of glucose on fsr-mediated biofilm formation in Enterococcus faecalis. J Infect Dis 190, 967–970.[CrossRef]
    [Google Scholar]
  43. Prakash, V. P. ( 2005; ). Clinical prevalence, identification and molecular characterization of enterococci. PhD thesis, Pondicherry University, India.
  44. Qin, X., Singh, K. V., Weinstock, G. M. & Murray, B. E. ( 2000; ). Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect Immun 68, 2579–2586.[CrossRef]
    [Google Scholar]
  45. Qin, X., Singh, K. V., Weinstock, G. M. & Murray, B. E. ( 2001; ). Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J Bacteriol 183, 3372–3382.[CrossRef]
    [Google Scholar]
  46. Raad, I. I., Hanna, H. A., Boktour, M., Chaiban, G., Hachem, R. Y., Dvorak, T., Lewis, R. & Murray, B. E. ( 2005; ). Vancomycin-resistant Enterococcus faecium: catheter colonization, esp gene, and decreased susceptibility to antibiotics in biofilm. Antimicrob Agents Chemother 49, 5046–5050.[CrossRef]
    [Google Scholar]
  47. Ramadhan, A. A. & Hegedus, E. ( 2005; ). Biofilm formation and esp gene carriage in enterococci. J Clin Pathol 58, 685–686.[CrossRef]
    [Google Scholar]
  48. Richards, M. J., Edwards, J. R., Culver, D. H. & Gaynes, R. P. ( 2000; ). Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol 21, 510–515.[CrossRef]
    [Google Scholar]
  49. Sandoe, J. A., Witherden, I. R., Cove, J. H., Heritage, J. & Wilcox, M. H. ( 2003; ). Correlation between enterococcal biofilm formation in vitro and medical-device-related infection potential in vivo. J Med Microbiol 52, 547–550.[CrossRef]
    [Google Scholar]
  50. Schauder, S., Shokat, K., Surette, M. G. & Bassler, B. L. ( 2001; ). The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41, 463–476.[CrossRef]
    [Google Scholar]
  51. Seno, Y., Kariyama, R., Mitsuhata, R., Monden, K. & Kumon, H. ( 2005; ). Clinical implications of biofilm formation by Enterococcus faecalis in the urinary tract. Acta Med Okayama 59, 79–87.
    [Google Scholar]
  52. Shankar, V., Baghdayan, A. S., Huycke, M. M., Lindahl, G. & 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.
    [Google Scholar]
  53. Shankar, N., Lockatell, C. V., Baghdayan, A. S., Drachenberg, C., Gilmore, M. S. & Johnson, D. E. ( 2001; ). Role of Enterococcus faecalis surface protein Esp in the pathogenesis of ascending urinary tract infection. Infect Immun 69, 4366–4372.[CrossRef]
    [Google Scholar]
  54. Sifri, C. D., Mylonakis, E., Singh, K. V., Qin, X., Garsin, D. A., Murray, B. E., Ausubel, F. M. & Calderwood, S. B. ( 2002; ). Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect Immun 70, 5647–5650.[CrossRef]
    [Google Scholar]
  55. Singh, K. V., Qin, X., Weinstock, G. M. & Murray, B. E. ( 1998; ). Generation and testing of mutants of Enterococcus faecalis in a mouse peritonitis model. J Infect Dis 178, 1416–1420.[CrossRef]
    [Google Scholar]
  56. Singh, K. V., Nallapareddy, S. R., Nannini, E. C. & Murray, B. E. ( 2005; ). Fsr-independent production of protease(s) may explain the lack of attenuation of an Enterococcus faecalis fsr mutant versus a gelE–sprE mutant in induction of endocarditis. Infect Immun 73, 4888–4894.[CrossRef]
    [Google Scholar]
  57. Tendolkar, P. M., Baghdayan, A. S., Gilmore, M. S. & Shankar, N. ( 2004; ). Enterococcal surface protein, Esp, enhances biofilm formation by Enterococcus faecalis. Infect Immun 72, 6032–6039.[CrossRef]
    [Google Scholar]
  58. Tendolkar, P. M., Baghdayan, A. S. & Shankar, N. ( 2005; ). The N-terminal domain of enterococcal surface protein, Esp, is sufficient for Esp-mediated biofilm enhancement in Enterococcus faecalis. J Bacteriol 187, 6213–6222.[CrossRef]
    [Google Scholar]
  59. Tendolkar, P. M., Baghdayan, A. S. & Shankar, N. ( 2006; ). Putative surface proteins encoded within a novel transferable locus confer a high-biofilm phenotype to Enterococcus faecalis. J Bacteriol 188, 2063–2072.[CrossRef]
    [Google Scholar]
  60. Toledo-Arana, A., Valle, J., Solano, C., Arrizubieta, M. J., Cucarella, C., Lamata, M., Amorena, B., Leiva, J., Penades, J. R. & Lasa, I. ( 2001; ). The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl Environ Microbiol 67, 4538–4545.[CrossRef]
    [Google Scholar]
  61. van Merode, A. E., van der Mei, H. C., Busscher, H. J. & Krom, B. P. ( 2006; ). Influence of culture heterogeneity in cell surface charge on adhesion and biofilm formation by Enterococcus faecalis. J Bacteriol 188, 2421–2426.[CrossRef]
    [Google Scholar]
  62. Van Wamel, W. J., Hendrickx, A. P., Bonten, M. J., Top, J., Posthuma, G. & Willems, R. J. ( 2007; ). Growth condition-dependent Esp expression by Enterococcus faecium affects initial adherence and biofilm formation. Infect Immun 75, 924–931.[CrossRef]
    [Google Scholar]
  63. Vuong, C., Saenz, H. L., Gotz, F. & Otto, M. ( 2000; ). Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J Infect Dis 182, 1688–1693.[CrossRef]
    [Google Scholar]
  64. Vuong, C., Kocianova, S., Yao, Y., Carmody, A. B. & Otto, M. ( 2004; ). Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo. J Infect Dis 190, 1498–1505.[CrossRef]
    [Google Scholar]
  65. Xu, Y., Singh, K. V., Qin, X., Murray, B. E. & Weinstock, G. M. ( 2000; ). Analysis of a gene cluster of Enterococcus faecalis involved in polysaccharide biosynthesis. Infect Immun 68, 815–823.[CrossRef]
    [Google Scholar]
  66. Zeng, J., Teng, F. & Murray, B. E. ( 2005; ). Gelatinase is important for translocation of Enterococcus faecalis across polarized human enterocyte-like T84 cells. Infect Immun 73, 1606–1612.[CrossRef]
    [Google Scholar]
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