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Challenges in the Eradication of Enterococcus faecalis and its Implications on Health

  • Microbiology (M Klein, Section Editor)
  • Published:
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Abstract

Enterococcus faecalis is frequently found in infected root canals of teeth with persistent apical periodontitis.

Purpose

To review the challenges involved in the eradication of persistent Enterococcus faecalis infections and their impact on human health.

Recent Findings

In the root canal system, Enterococcus faecalis resides in biofilm communities that are able to resist a wide range of harsh conditions and treatments and persist for years. Various virulence and resistance factors provide Enterococcus faecalis capabilities in adherence, colonization, and biofilm formation, which is much more resistant to antibacterial agents than planktonic bacteria. These capabilities explain its persistence in root canal infections. To date, the available therapeutic tools to efficiently eradicate Enterococcus faecalis infections remain limited. Recently, in a model mimicking Enterococcus faecalis root canal infection, novel biofilm inhibitors and dispersing agents, such as D-Leucine, presented superior capability over sodium hypochlorite, the frequently used root-canal antibacterial irrigation solution, in the eradication of Enterococcus faecalis.

Summary

These recent studies present promising treatment regimens for Enterococcus faecalis persistent infections.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Annu Rev Microbiol. 2002;56(1):187–209. https://doi.org/10.1146/annurev.micro.56.012302.160705.

    Article  CAS  PubMed  Google Scholar 

  2. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol. 2001;55(1):165–99. https://doi.org/10.1146/annurev.micro.55.1.165.

    Article  CAS  PubMed  Google Scholar 

  3. Aguilar C, Vlamakis H, Losick R, Kolter R. Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol. 2007;10(6):638–43. https://doi.org/10.1016/j.mib.2007.09.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kolter R, Greenberg EP. Microbial sciences: the superficial life of microbes. Nature. 2006;441(7091):300–2. https://doi.org/10.1038/441300a.

    Article  CAS  PubMed  Google Scholar 

  5. Branda SS, Vik S, Friedman L, Kolter R. Biofilms: the matrix revisited. Trends Microbiol. 2005;13(1):20–6. https://doi.org/10.1016/j.tim.2004.11.006.

    Article  CAS  PubMed  Google Scholar 

  6. Oppenheimer-Shaanan Y, Steinberg N, Kolodkin-Gal I. Small molecules are natural triggers for the disassembly of biofilms. Trends Microbiol. 2013;21(11):594–601. https://doi.org/10.1016/j.tim.2013.08.005.

    Article  CAS  PubMed  Google Scholar 

  7. Parsek MR, Singh PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol. 2003;57(1):677–701. https://doi.org/10.1146/annurev.micro.57.030502.090720.

    Article  CAS  PubMed  Google Scholar 

  8. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol. 2013;11(3):157–68. https://doi.org/10.1038/nrmicro2960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. • Rosen E, Tsesis I, Elbahary S, Storzi N, Kolodkin-Gal I. Eradication of Enterococcus faecalis biofilms on human dentin. Front Microbiol. 2016;7:2055. https://doi.org/10.3389/fmicb.2016.02055.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15(2):167–93. https://doi.org/10.1128/CMR.15.2.167-193.2002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318–22. https://doi.org/10.1126/science.284.5418.1318.

    Article  CAS  PubMed  Google Scholar 

  12. Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol. 2005;13(1):34–40. https://doi.org/10.1016/j.tim.2004.11.010.

    Article  CAS  PubMed  Google Scholar 

  13. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O’Toole GA. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature. 2003;426(6964):306–10. https://doi.org/10.1038/nature02122.

    Article  CAS  PubMed  Google Scholar 

  14. Stewart PS. Biofilm accumulation model that predicts antibiotic resistance of Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother. 1994;38(5):1052–8. https://doi.org/10.1128/AAC.38.5.1052.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Stewart PS. Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol : IJMM. 2002;292(2):107–13. https://doi.org/10.1078/1438-4221-00196.

    Article  CAS  PubMed  Google Scholar 

  16. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135–8. https://doi.org/10.1016/S0140-6736(01)05321-1.

    Article  CAS  PubMed  Google Scholar 

  17. Khalifa L, Brosh Y, Gelman D, Coppenhagen-Glazer S, Beyth S, Poradosu-Cohen R, et al. Targeting Enterococcus faecalis biofilms with phage therapy. Appl Environ Microbiol. 2015;81(8):2696–705. https://doi.org/10.1128/AEM.00096-15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Deshpande LM, Fritsche TR, Moet GJ, Biedenbach DJ, Jones RN. Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program. Diagn Microbiol Infect Dis. 2007;58(2):163–70. https://doi.org/10.1016/j.diagmicrobio.2006.12.022.

    Article  CAS  PubMed  Google Scholar 

  19. Haapasalo M, Shen YA. Current therapeutic options for endodontic biofilms. Endod Top. 2012;22:79–98.

    Article  Google Scholar 

  20. Ricucci D, Siqueira JF Jr. Biofilms and apical periodontitis: study of prevalence and association with clinical and histopathologic findings. J Endod. 2010;36(8):1277–88. https://doi.org/10.1016/j.joen.2010.04.007.

    Article  PubMed  Google Scholar 

  21. Zhang CJ, Du JR, Peng ZX. Correlation between Enterococcus faecalis and persistent Intraradicular infection compared with primary intraradicular infection: a systematic review. J Endod. 2015;41(8):1207–13. https://doi.org/10.1016/j.joen.2015.04.008.

    Article  PubMed  Google Scholar 

  22. Meire MA, Coenye T, Nelis HJ, De Moor RJ. Evaluation of Nd:YAG and Er:YAG irradiation, antibacterial photodynamic therapy and sodium hypochlorite treatment on Enterococcus faecalis biofilms. Int Endod J. 2012;45(5):482–91. https://doi.org/10.1111/j.1365-2591.2011.02000.x.

    Article  CAS  PubMed  Google Scholar 

  23. Du T, Shi Q, Shen Y, Cao Y, Ma J, Lu X, et al. Effect of modified nonequilibrium plasma with chlorhexidine digluconate against endodontic biofilms in vitro. J Endod. 2013;39(11):1438–43. https://doi.org/10.1016/j.joen.2013.06.027.

    Article  PubMed  Google Scholar 

  24. Tay CX, Quah SY, Lui JN, VS Y, Tan KS. Matrix metalloproteinase inhibitor as an antimicrobial agent to eradicate Enterococcus faecalis biofilm. J Endod. 2015;41(6):858–63. https://doi.org/10.1016/j.joen.2015.01.032.

    Article  PubMed  Google Scholar 

  25. Anderson AC, Jonas D, Huber I, Karygianni L, Wolber J, Hellwig E, et al. Enterococcus faecalis from food, clinical specimens, and oral sites: prevalence of virulence factors in association with biofilm formation. Front Microbiol. 2015;6:1534. https://doi.org/10.3389/fmicb.2015.01534.

    PubMed  Google Scholar 

  26. John G, Kumar KP, Gopal SS, Kumari S, Reddy BK. Enterococcus faecalis, a nightmare to endodontist: a systematic review. Afr J Microbiol Res. 2015:898–908.

  27. Sjolund M, Wreiber K, Andersson DI, Blaser MJ, Engstrand L. Long-term persistence of resistant Enterococcus species after antibiotics to eradicate Helicobacter pylori. Ann Intern Med. 2003;139(6):483–7. https://doi.org/10.7326/0003-4819-139-6-200309160-00011.

    Article  PubMed  Google Scholar 

  28. Agudelo Higuita NI, Huycke MM. Enterococcal disease, epidemiology, and implications for treatment. In: Gilmore MS, Clewell DB, Ike Y, Shankar N, editors. Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. Boston2014.

  29. Noskin GA, Peterson LR, Warren JR. Enterococcus faecium and Enterococcus faecalis bacteremia: acquisition and outcome. Clin Infect Dis. 1995;20(2):296–301. https://doi.org/10.1093/clinids/20.2.296.

    Article  CAS  PubMed  Google Scholar 

  30. Huycke MM, Sahm DF, Gilmore MS. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis. 1998;4(2):239–49. https://doi.org/10.3201/eid0402.980211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kim JY, Song HS, Kim YB, Kwon J, Choi JS, Cho YJ, et al. Genome sequence of a commensal bacterium, Enterococcus faecalis CBA7120, isolated from a Korean fecal sample. Gut Pathog. 2016;8(1):62. https://doi.org/10.1186/s13099-016-0145-x.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Evans AC, Chinn AL. The Enterococci: with special reference to their association with human disease. J Bacteriol. 1947;54(4):495–512.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Lancefield RC. A serological differentiation of human and other groups of hemolytic streptococci. J Exp Med. 1933;57(4):571–95. https://doi.org/10.1084/jem.57.4.571.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Fleming A. On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. Br J Exp Pathol. 1929;10:226–36.

    CAS  PubMed Central  Google Scholar 

  35. Sherman JM. The streptococci. Bacteriol Rev. 1937;1(1):3–97.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. E J, Jiang YT, Yan PF, Liang JP. Biological changes of Enterococcus faecalis in the viable but nonculturable state. Genet Mol Res : GMR. 2015;14(4):14790–801. https://doi.org/10.4238/2015.November.18.44.

    Article  CAS  PubMed  Google Scholar 

  37. Souto R, Colombo AP. Prevalence of Enterococcus faecalis in subgingival biofilm and saliva of subjects with chronic periodontal infection. Arch Oral Biol. 2008;53(2):155–60. https://doi.org/10.1016/j.archoralbio.2007.08.004.

    Article  CAS  PubMed  Google Scholar 

  38. Flanagan D. Enterococcus faecalis and dental implants. J Oral Implantol. 2017;43(1):8–11. https://doi.org/10.1563/aaid-joi-D-16-00069.

    Article  PubMed  Google Scholar 

  39. Kouidhi B, Zmantar T, Mahdouani K, Hentati H, Bakhrouf A. Antibiotic resistance and adhesion properties of oral Enterococci associated to dental caries. BMC Microbiol. 2011;11(1):155. https://doi.org/10.1186/1471-2180-11-155.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Molander A, Reit C, Dahlen G, Kvist T. Microbiological status of root-filled teeth with apical periodontitis. Int Endod J. 1998;31(1):1–7. https://doi.org/10.1046/j.1365-2591.1998.t01-1-00111.x.

    Article  CAS  PubMed  Google Scholar 

  41. Zapata RO, Branante CM, de Moraes IG, Bernardineli N, Gasparoto TH, Graeff MSZ, et al. Confocal laser scanning microscopy is appropriate to detect viability of Enterococcus faecalis in infected dentin. J Endod. 2008;34(10):1198–201. https://doi.org/10.1016/j.joen.2008.07.001.

    Article  PubMed  Google Scholar 

  42. Paganelli FL, Willems RJ, Leavis HL. Optimizing future treatment of enterococcal infections: attacking the biofilm? Trends Microbiol. 2012;20(1):40–9. https://doi.org/10.1016/j.tim.2011.11.001.

    Article  CAS  PubMed  Google Scholar 

  43. Bryers JD. Medical biofilms. Biotechnol Bioeng. 2008;100(1):1–18. https://doi.org/10.1002/bit.21838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wang QQ, Zhang CF, Chu CH, Zhu XF. Prevalence of Enterococcus faecalis in saliva and filled root canals of teeth associated with apical periodontitis. Int J Oral Sci. 2012;4(1):19–23. https://doi.org/10.1038/ijos.2012.17.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Kishen A. Advanced therapeutic options for endodontic biofilms. Endod Top. 2012;22:99–123.

    Article  Google Scholar 

  46. Banin E, Vasil ML, Greenberg EP. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A. 2005;102(31):11076–81. https://doi.org/10.1073/pnas.0504266102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kolodkin-Gal I, Elsholz AK, Muth C, Girguis PR, Kolter R, Losick R. Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase. Genes Dev. 2013;27(8):887–99. https://doi.org/10.1101/gad.215244.113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ramos I, Dietrich LE, Price-Whelan A, Newman DK. Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res Microbiol. 2010;161(3):187–91. https://doi.org/10.1016/j.resmic.2010.01.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Singh PK, Parsek MR, Greenberg EP, Welsh MJ. A component of innate immunity prevents bacterial biofilm development. Nature. 2002;417(6888):552–5. https://doi.org/10.1038/417552a.

    Article  CAS  PubMed  Google Scholar 

  50. Raad I, Chatzinikolaou I, Chaiban G, Hanna H, Hachem R, Dvorak T, et al. In vitro and ex vivo activities of minocycline and EDTA against microorganisms embedded in biofilm on catheter surfaces. Antimicrob Agents Chemother. 2003;47(11):3580–5. https://doi.org/10.1128/AAC.47.11.3580-3585.2003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. de Almeida J, Hoogenkamp M, Felippe WT, Crielaard W, van der Waal SV. Effectiveness of EDTA and modified salt solution to detach and kill cells from Enterococcus faecalis biofilm. J Endod. 2016;42(2):320–3. https://doi.org/10.1016/j.joen.2015.11.017.

    Article  PubMed  Google Scholar 

  52. Wong AW, Tsang CS, Zhang S, Li KY, Zhang C, Chu CH. Treatment outcomes of single-visit versus multiple-visit non-surgical endodontic therapy: a randomised clinical trial. BMC Oral Health. 2015;15(1):162. https://doi.org/10.1186/s12903-015-0148-x.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Wong AW, Zhang C, Chu CH. A systematic review of nonsurgical single-visit versus multiple-visit endodontic treatment. Clin Cosmet Investig Dent. 2014;6:45–56. https://doi.org/10.2147/CCIDE.S61487.

    PubMed  PubMed Central  Google Scholar 

  54. Manfredi M, Figini L, Gagliani M, Lodi G. Single versus multiple visits for endodontic treatment of permanent teeth. Cochrane Database Syst Rev. 2016;12:CD005296. https://doi.org/10.1002/14651858.CD005296.pub3.

    PubMed  Google Scholar 

  55. Kim S, Kratchman S. Modern endodontic surgery concepts and practice: a review. J Endod. 2006;32(7):601–23. https://doi.org/10.1016/j.joen.2005.12.010.

    Article  PubMed  Google Scholar 

  56. Tsesis I, Rosen E, Schwartz-Arad D, Fuss Z. Retrospective evaluation of surgical endodontic treatment: traditional versus modern technique. J Endod. 2006;32(5):412–6. https://doi.org/10.1016/j.joen.2005.10.051.

    Article  PubMed  Google Scholar 

  57. Rubinstein RAKS. Short-term observation of the results of endodontic surgery with the use of surgical operation microscope and super-EBA as root end filling material. J Endod. 1999;25(1):43–8. https://doi.org/10.1016/S0099-2399(99)80398-7.

    Article  Google Scholar 

  58. Tsesis I, Faivishevsky V, Kfir A, Rosen E. Outcome of surgical endodontic treatment performed by a modern technique: a meta-analysis of literature. J Endod. 2009;35(11):1505–11. https://doi.org/10.1016/j.joen.2009.07.025.

    Article  PubMed  Google Scholar 

  59. Gartner AH, Dorn SO. Advances in endodontic surgery. Dent Clin N Am. 1992;36(2):357–78.

    CAS  PubMed  Google Scholar 

  60. • Tsesis I, Elbahary S, Venezia NB, Rosen E. Bacterial colonization in the apical part of extracted human teeth following root-end resection and filling: a confocal laser scanning microscopy study. Clin Oral Investig. 2017;22(1):267–74. https://doi.org/10.1007/s00784-017-2107-1.

    Article  PubMed  Google Scholar 

  61. Peters LB, Wesselink PR, Buijs JF, van Winkelhoff AJ. Viable bacteria in root dentinal tubules of teeth with apical periodontitis. J Endod. 2001;27(2):76–81. https://doi.org/10.1097/00004770-200102000-00002.

    Article  CAS  PubMed  Google Scholar 

  62. Saleh IM, Ruyter IE, Haapasalo M, Orstavik D. Survival of Enterococcus faecalis in infected dentinal tubules after root canal filling with different root canal sealers in vitro. Int Endod J. 2004;37(3):193–8. https://doi.org/10.1111/j.0143-2885.2004.00785.x.

    Article  CAS  PubMed  Google Scholar 

  63. del Carpio-Perochena A, Bramante CM, de Andrade FB, Maliza AG, Cavenago BC, Marciano MA, et al. Antibacterial and dissolution ability of sodium hypochlorite in different pHs on multi-species biofilms. Clin Oral Investig. 2015;19(8):2067–73. https://doi.org/10.1007/s00784-015-1431-6.

    Article  PubMed  Google Scholar 

  64. Louwakul P, Saelo A, Khemaleelakul S. Efficacy of calcium oxide and calcium hydroxide nanoparticles on the elimination of Enterococcus faecalis in human root dentin. Clin Oral Investig. 2016;21(3):865–71. https://doi.org/10.1007/s00784-016-1836-x.

    Article  PubMed  Google Scholar 

  65. Slutzky H, Slutzky-Goldberg I, Weiss EI, Matalon S. Antibacterial properties of temporary filling materials. J Endod. 2006;32(3):214–7. https://doi.org/10.1016/j.joen.2005.10.034.

    Article  PubMed  Google Scholar 

  66. Chong BS, Owadally ID, Pitt Ford TR, Wilson RF. Antibacterial activity of potential retrograde root filling materials. Endod Dent Traumatol. 1994;10(2):66–70. https://doi.org/10.1111/j.1600-9657.1994.tb00062.x.

    Article  CAS  PubMed  Google Scholar 

  67. Grech L, Mallia B, Camilleri J. Characterization of set intermediate restorative material, biodentine, bioaggregate and a prototype calcium silicate cement for use as root-end filling materials. Int Endod J. 2013;46(7):632–41. https://doi.org/10.1111/iej.12039.

    Article  CAS  PubMed  Google Scholar 

  68. Malkondu O, Karapinar Kazandag M, Kazazoglu EA. Review on biodentine, a contemporary dentine replacement and repair material. Biomed Res Int. 2014;2014:160951. https://doi.org/10.1155/2014/160951.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Naik MM, de Ataide Ide N, Fernandes M, Lambor R. Assessment of apical seal obtained after irrigation of root end cavity with MTAD followed by subsequent retrofilling with MTA and biodentine: an in vitro study. J Conserv Dent. 2015;18(2):132–5. https://doi.org/10.4103/0972-0707.153068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ravichandra PV, Vemisetty H, Deepthi K, Reddy SJ, Ramkiran D, Krishna MJ, et al. Comparative evaluation of marginal adaptation of biodentine(TM) and other commonly used root end filling materials-an in vitro study. J Clin Diagn Res. 2014;8(3):243–5. https://doi.org/10.7860/JCDR/2014/7834.4174.

    Google Scholar 

  71. Rajasekharan S, Martens LC, Cauwels RG, Verbeeck RM. Biodentine material characteristics and clinical applications: a review of the literature. Eur Arch Paediatr Dent. 2014;15(3):147–58. https://doi.org/10.1007/s40368-014-0114-3.

    Article  CAS  PubMed  Google Scholar 

  72. Soundappan S, Sundaramurthy JL, Raghu S, Natanasabapathy V. Biodentine versus mineral trioxide aggregate versus intermediate restorative material for retrograde root end filling: an in vitro study. J Dent (Tehran). 2014;11(2):143–9.

    Google Scholar 

  73. Newberry BM, Shabahang S, Johnson N, Aprecio RM, Torabinejad M. The antimicrobial effect of biopure MTAD on eight strains of Enterococcus faecalis: an in vitro investigation. J Endod. 2007;33(11):1352–4. https://doi.org/10.1016/j.joen.2007.07.006.

    Article  PubMed  Google Scholar 

  74. Giardino L, Ambu E, Savoldi E, Rimondini R, Cassanelli C, Debbia EA. Comparative evaluation of antimicrobial efficacy of sodium hypochlorite, MTAD, and Tetraclean against Enterococcus faecalis biofilm. J Endod. 2007;33(7):852–5. https://doi.org/10.1016/j.joen.2007.02.012.

    Article  PubMed  Google Scholar 

  75. Zhang R, Chen M, Lu Y, Guo X, Qiao F, Wu L. Antibacterial and residual antimicrobial activities against Enterococcus faecalis biofilm: a comparison between EDTA, chlorhexidine, cetrimide, MTAD and QMix. Sci Rep. 2015;5(1):12944. https://doi.org/10.1038/srep12944.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Rodig T, Endres S, Konietschke F, Zimmermann O, Sydow HG, Wiegand A. Effect of fiber insertion depth on antibacterial efficacy of photodynamic therapy against Enterococcus faecalis in rootcanals. Clin Oral Investig. 2017;21(5):1753–9. https://doi.org/10.1007/s00784-016-1948-3.

    Article  PubMed  Google Scholar 

  77. Dengler V, Meier PS, Heusser R, Berger-Bachi B, McCallum N. Induction kinetics of the Staphylococcus aureus cell wall stress stimulon in response to different cell wall active antibiotics. BMC Microbiol. 2011;11(1):16. https://doi.org/10.1186/1471-2180-11-16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. • Bucher T, Oppenheimer-Shaanan Y, Savidor A, Bloom-Ackermann Z, Kolodkin-Gal I. Disturbance of the bacterial cell wall specifically interferes with biofilm formation. Environ Microbiol Rep. 2015;7(6):990–1004. https://doi.org/10.1111/1758-2229.12346.

    Article  CAS  PubMed  Google Scholar 

  79. Lam H, DC O, Cava F, Takacs CN, Clardy J, de Pedro MA, et al. D-amino acids govern stationary phase cell wall remodeling in bacteria. Science. 2009;325(5947):1552–5. https://doi.org/10.1126/science.1178123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Cava F, de Pedro MA, Lam H, Davis BM, Waldor MK. Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J. 2011;30(16):3442–53. https://doi.org/10.1038/emboj.2011.246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Lupoli TJ, Tsukamoto H, Doud EH, Wang TS, Walker S, Kahne D. Transpeptidase-mediated incorporation of D-amino acids into bacterial peptidoglycan. J Am Chem Soc. 2011;133(28):10748–51. https://doi.org/10.1021/ja2040656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. • Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R. D-amino acids trigger biofilm disassembly. Science. 2010;328(5978):627–9. https://doi.org/10.1126/science.1188628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Hochbaum AI, Kolodkin-Gal I, Foulston L, Kolter R, Aizenberg J, Losick R. Inhibitory effects of D-amino acids on Staphylococcus aureus biofilm development. J Bacteriol. 2011;193(20):5616–22. https://doi.org/10.1128/JB.05534-11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Sanchez CJ Jr, Prieto EM, Krueger CA, Zienkiewicz KJ, Romano DR, Ward CL, et al. Effects of local delivery of d-amino acids from biofilm-dispersive scaffolds on infection in contaminated rat segmental defects. Biomaterials. 2013;34(30):7533–43. https://doi.org/10.1016/j.biomaterials.2013.06.026.

    Article  CAS  PubMed  Google Scholar 

  85. Yu C, Wu JJ, Contreras AE, Li QL. Control of nanofiltration membrane biofouling by Pseudomonas aeruginosa using D-tyrosine. J Membr Sci. 2012;423:487–94. https://doi.org/10.1016/j.memsci.2012.08.051.

    Article  Google Scholar 

  86. She P, Chen L, Liu H, Zou Y, Luo Z, Koronfel A, et al. The effects of d-Tyrosine combined with amikacin on the biofilms of Pseudomonas aeruginosa. Microb Pathog. 2015;86:38–44. https://doi.org/10.1016/j.micpath.2015.07.009.

    Article  CAS  PubMed  Google Scholar 

  87. Li J, Wang N. Foliar application of biofilm formation-inhibiting compounds enhances control of citrus canker caused by Xanthomonas citri subsp. citri. Phytopathology. 2014;104(2):134–42. https://doi.org/10.1094/PHYTO-04-13-0100-R.

    Article  CAS  PubMed  Google Scholar 

  88. Koch AL. Microbial physiology and ecology of slow growth. Microbiol Mol Biol Rev : MMBR. 1997;61(3):305–18.

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Hiyari S, Bennett KM. Dental diagnostics: molecular analysis of oral biofilms. J Dent Hyg : JDH / Am Dent Hyg Assoc. 2011;85(4):256–63.

    Google Scholar 

  90. Harmata AJ, Ma Y, Sanchez CJ, Zienkiewicz KJ, Elefteriou F, Wenke JC, et al. D-amino acid inhibits biofilm but not new bone formation in an ovine model. Clin Orthop Relat Res. 2015;473(12):3951–61. https://doi.org/10.1007/s11999-015-4465-9.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Tsume Y, Incecayir T, Song X, Hilfinger JM, Amidon GL. The development of orally administrable gemcitabine prodrugs with D-enantiomer amino acids: enhanced membrane permeability and enzymatic stability. Eur J Pharm Biopharm : Off J Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik eV. 2014;86(3):514–23. https://doi.org/10.1016/j.ejpb.2013.12.009.

    Article  CAS  Google Scholar 

  92. Kolodkin-Gal I. Beyond the wall: can D-amino acids and small molecule inhibitors eliminate infections? Future Med Chem. 2017;9(9):843–6. https://doi.org/10.4155/fmc-2017-0069.

    Article  CAS  PubMed  Google Scholar 

  93. Zilm PS, Butnejski V, Rossi-Fedele G, Kidd SP, Edwards S, Vasilev K. D-amino acids reduce Enterococcus faecalis biofilms in vitro and in the presence of antimicrobials used for root canal treatment. PLoS One. 2017;12(2):e0170670. https://doi.org/10.1371/journal.pone.0170670.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Kaes C, Katz A, Hosseini MW. Bipyridine: the most widely used ligand. A review of molecules comprising at least two 2,2 '-bipyridine units. Chem Rev. 2000;100(10):3553–90. https://doi.org/10.1021/cr990376z.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Eyal Rosen.

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Rosen, E., Kolodkin-Gal, I. & Tsesis, I. Challenges in the Eradication of Enterococcus faecalis and its Implications on Health. Curr Oral Health Rep 5, 70–77 (2018). https://doi.org/10.1007/s40496-018-0172-4

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