Targeting Enterococcus faecalis biofilms with phage therapy

Applied and Environmental Microbiology

Volumn 81, Issue 8, 2015, Pages 2696-2705

  Khalifa, Leron ^a   Brosh, Yair ^a   Gelman, Daniel ^a   Coppenhagen Glazer, Shunit ^a   Beyth, Shaul ^b   Poradosu Cohen, Ronit ^c   Que, Yok Ai ^d   Beyth, Nurit ^a   Hazan, Ronen ^a,e  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c TEL AVIV UNIVERSITY   (Israel)

^d LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^e Israel Institute for Advanced Research IYAR   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACILLI; BACTERIA; BACTERIOPHAGES; BIOFILMS; BIOLOGY; GENES; HYDRAULIC STRUCTURES; PATHOGENS; SEWAGE;

ANTIBACTERIAL EFFICACY; ANTIBIOTIC RESISTANCE; ENTEROCOCCUS FAECALIS; GRAM-POSITIVE PATHOGENS; MULTIDRUG RESISTANTS; PERSISTENT INFECTION; ROOT CANAL TREATMENT; WHOLE GENOME SEQUENCING;

DRUG THERAPY;

ANTIBIOTICS; BACTERIUM; BIOFILM; DRUG RESISTANCE; EMERGENCE; INFECTIOUS DISEASE; PHYLOGENY; PLANKTON;

ENTEROCOCCUS FAECALIS; MYOVIRIDAE; POSIBACTERIA;

SEWAGE;

BIOFILM; DENTAL PULP DISEASES; DNA SEQUENCE; ENTEROCOCCUS FAECALIS; GENETICS; GRAM-POSITIVE BACTERIAL INFECTIONS; MICROBIOLOGY; MOLECULAR GENETICS; MYOVIRIDAE; PHYSIOLOGY; PLANKTON; SEWAGE; TOOTH PULP; VIROLOGY; VIRUS GENOME;

BIOFILMS; DENTAL PULP CAVITY; DENTAL PULP DISEASES; ENTEROCOCCUS FAECALIS; GENOME, VIRAL; GRAM-POSITIVE BACTERIAL INFECTIONS; MOLECULAR SEQUENCE DATA; MYOVIRIDAE; PLANKTON; SEQUENCE ANALYSIS, DNA; SEWAGE;

EID: 84927784673     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00096-15     Document Type: Article

References (54)

1. Dahl A, Bruun NE. 2013. Enterococcus faecalis infective endocarditis: focus on clinical aspects. Expert Rev Cardiovasc Ther 11:1247-1257. http://dx.doi.org/10.1586/14779072.2013.832482.
2. Stuart CH, Schwartz SA, Beeson TJ, Owatz CB. 2006. Enterococcus faecalis: its role in root canal treatment failure and current concepts in retreatment. J Endod 32:93-98. http://dx.doi.org/10.1016/j.joen.2005.10.049.
3. Tebruegge M, Pantazidou A, Clifford V, Gonis G, Ritz N, Connell T, Curtis N. 2011. The age-related risk of coexisting meningitis in children with urinary tract infection. PLoS One 6:e26576. http://dx.doi.org/10.1371/journal.pone.0026576.
4. Koch S, Hufnagel M, Theilacker C, Huebner J. 2004. Enterococcal infections: host response, therapeutic, and prophylactic possibilities. Vaccine 22:822-830. http://dx.doi.org/10.1016/j.vaccine.2003.11.027.
5. Molander A, Reit C, Dahlen G, Kvist T. 1998. Microbiological status of root-filled teeth with apical periodontitis. Int Endod J 31:1-7. http://dx.doi.org/10.1046/j.1365-2591.1998.t01-1-00111.x.
6. Wang QQ, Zhang CF, Chu CH, Zhu XF. 2012. Prevalence of Enterococcus faecalis in saliva and filled root canals of teeth associated with apical periodontitis. Int J Oral Sci 4:19-23. http://dx.doi.org/10.1038/ijos.2012.17.
7. Siqueira JF, Jr, Rocas IN, Ricucci D, Hulsmann M. 2014. Causes and management of post-treatment apical periodontitis. Br Dent J 216:305-312. http://dx.doi.org/10.1038/sj.bdj.2014.200.
8. Waltimo T, Trope M, Haapasalo M, Orstavik D. 2005. Clinical efficacy of treatment procedures in endodontic infection control and one-year follow-up of periapical healing. J Endod 31:863-866. http://dx.doi.org/10.1097/01.don.0000164856.27920.85.
9. Lewis K. 2001. Riddle of biofilm resistance. Antimicrob Agents Chemother 45:999-1007. http://dx.doi.org/10.1128/AAC.45.4.999-1007.2001.
10. Campoccia D, Montanaro L, Arciola CR. 2006. The significance of infection related to orthopedic devices and issues of antibiotic resistance. Biomaterials 27:2331-2339. http://dx.doi.org/10.1016/j.biomaterials.2005.11.044.
11. Li X, Kolltveit KM, Tronstad L, Olsen I. 2000. Systemic diseases caused by oral infection. Clin Microbiol Rev 13:547-558. http://dx.doi.org/10.1128/CMR.13.4.547-558.2000.
12. Ciofu O, Tolker-Nielsen T, Jensen PO, Wang H, Hoiby N. 2014. Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Adv Drug Delivery Rev http://dx.doi.org/10.1016/j.addr.2014.11.017.
13. Walsh FM, Amyes SG. 2004. Microbiology and drug resistance mechanisms of fully resistant pathogens. Curr Opin Microbiol 7:439-444. http://dx.doi.org/10.1016/j.mib.2004.08.007.
14. Beloin C, Renard S, Ghigo JM, Lebeaux D. 2014. Novel approaches to combat bacterial biofilms. Curr Opin Pharmacol 18C:61-68. http://dx.doi.org/10.1016/j.coph.2014.09.005.
15. Brooks BD, Brooks AE. 2014. Therapeutic strategies to combat antibiotic resistance. Adv Drug Delivery Rev 78C:14-27. http://dx.doi.org/10.1016/j.addr.2014.10.027.
16. Rani SA, Pitts B, Stewart PS. 2005. Rapid diffusion of fluorescent tracers into Staphylococcus epidermidis biofilms visualized by time lapse microscopy. Antimicrob Agents Chemother 49:728-732. http://dx.doi.org/10.1128/AAC.49.2.728-732.2005.
17. Stewart PS. 2003. Diffusion in biofilms. J Bacteriol 185:1485-1491. http://dx.doi.org/10.1128/JB.185.5.1485-1491.2003.
18. Vega NM, Gore J. 2014. Collective antibiotic resistance: mechanisms and implications. Curr Opin Microbiol 21C:28-34. http://dx.doi.org/10.1016/j.mib.2014.09.003.
19. Matsuzaki S, Uchiyama J, Takemura-Uchiyama I, Daibata M. 2014. Perspective: the age of the phage. Nature 509:S9. http://dx.doi.org/10.1038/509S9a.
20. Reardon S. 2014. Phage therapy gets revitalized. Nature 510:15-16. http://dx.doi.org/10.1038/510015a.
21. Chanishvili N. 2012. Phage therapy: history from Twort and d'Herelle through Soviet experience to current approaches. Adv Virus Res 83:3-40. http://dx.doi.org/10.1016/B978-0-12-394438-2.00001-3.
22. Fruciano DE, Bourne S. 2007. Phage as an antimicrobial agent: d'Herelle's heretical theories and their role in the decline of phage prophylaxis in the West. Can J Infect Dis Med Microbiol 18:19-26.
23. Thiel K. 2004. Old dogma, new tricks-21st Century phage therapy. Nat Biotechnol 22:31-36. http://dx.doi.org/10.1038/nbt0104-31.
24. Häusler T. 2006. Viruses versus superbugs: a solution to the antibiotics crisis?, 2nd ed. Palgrave Macmillan, New York, NY.
25. Sarhan WA, Azzazy HM. 2015. Phage approved in food, why not as a therapeutic? Expert Rev Anti-Infect Ther 13:91-101. http://dx.doi.org/10.1586/14787210.2015.990383.
26. Yilmaz C, Colak M, Yilmaz BC, Ersoz G, Kutateladze M, Gozlugol M. 2013. Bacteriophage therapy in implant-related infections: an experimental study. J Bone Joint Surg 95:117-125. http://dx.doi.org/10.2106/JBJS.K.01135.
27. Kamal F, Dennis JJ. 2015. Burkholderia cepacia complex phage-antibiotic synergy (PAS): antibiotics stimulate lytic phage activity. Appl Environ Microbiol 81:1132-1138. http://dx.doi.org/10.1128/AEM.02850-14.
28. Coulter LB, McLean RJ, Rohde RE, Aron GM. 2014. Effect of bacteriophage infection in combination with tobramycin on the emergence of resistance in Escherichia coli and Pseudomonas aeruginosa biofilms. Viruses 6:3778-3786. http://dx.doi.org/10.3390/v6103778.
29. Kumari S, Harjai K, Chhibber S. 2011. Bacteriophage versus antimicrobial agents for the treatment of murine burn wound infection caused by Klebsiella pneumoniae B5055. J Med Microbiol 60:205-210. http://dx.doi.org/10.1099/jmm.0.018580-0.
30. Wright A, Hawkins CH, Anggard EE, Harper DR. 2009. A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin Otolaryngol 34:349-357. http://dx.doi.org/10.1111/j.1749-4486.2009.01973.x.
31. Stevens RH, Porras OD, Delisle AL. 2009. Bacteriophages induced from lysogenic root canal isolates of Enterococcus faecalis. Oral Microbiol Immunol 24:278-284. http://dx.doi.org/10.1111/j.1399-302X.2009.00506.x.
32. Paisano AF, Spira B, Cai S, Bombana AC. 2004. In vitro antimicrobial effect of bacteriophages on human dentin infected with Enterococcus faecalis ATCC 29212. Oral Microbiol Immunol 19:327-330. http://dx.doi.org/10.1111/j.1399-302x.2004.00166.x.
33. Clokie MRJ, Kropinski AM. 2009. Bacteriophages: methods and protocols. Humana Press, New York, NY.
34. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 40:175-179. http://dx.doi.org/10.1016/S0167-7012(00)00122-6.
35. Kot W, Vogensen FK, Sorensen SJ, Hansen LH. 2013. DPS: a rapid method for genome sequencing of DNA-containing bacteriophages directly from a single plaque. J Virol Methods 196C:152-156. http://dx.doi.org/10.1016/j.jviromet.2013.10.040.
36. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676. http://dx.doi.org/10.1093/bioinformatics/bti610.
37. Henry DA, Campbell ME, LiPuma JJ, Speert DP. 1997. Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J Clin Microbiol 35:614-619.
38. Wolanek GA, Loushine RJ, Weller RN, Kimbrough WF, Volkmann KR. 2001. In vitro bacterial penetration of endodontically treated teeth coronally sealed with a dentin bonding agent. J Endod 27:354-357. http://dx.doi.org/10.1097/00004770-200105000-00012.
39. de la Fuente-Nunez C, Reffuveille F, Fernandez L, Hancock RE. 2013. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 16:580-589. http://dx.doi.org/10.1016/j.mib.2013.06.013.
40. Klumpp J, Lavigne R, Loessner MJ, Ackermann HW. 2010. The SPO1-related bacteriophages. Arch Virol 155:1547-1561. http://dx.doi.org/10.1007/s00705-010-0783-0.
41. Zink R, Loessner MJ. 1992. Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Appl Environ Microbiol 58:296-302.
42. Uchiyama J, Rashel M, Takemura I, Wakiguchi H, Matsuzaki S. 2008. In silico and in vivo evaluation of bacteriophage phiEF24c, a candidate for treatment of Enterococcus faecalis infections. Appl Environ Microbiol 74: 4149-4163. http://dx.doi.org/10.1128/AEM.02371-07.
43. Conesa A, Gotz S. 2008. Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832. http://dx.doi.org/10.1155/2008/619832.
44. Li X, Ding P, Han C, Fan H, Wang Y, Mi Z, Feng F, Tong Y. 2014. Genome analysis of Enterococcus faecalis bacteriophage IME-EF3 harboring a putative metallo-beta-lactamase gene. Virus Genes 49:145-151. http://dx.doi.org/10.1007/s11262-014-1079-3.
45. Lobocka M, Hejnowicz MS, Dabrowski K, Gozdek A, Kosakowski J, Witkowska M, Ulatowska MI, Weber-Dabrowska B, Kwiatek M, Parasion S, Gawor J, Kosowska H, Glowacka A. 2012. Genomics of staphylococcal Twort-like phages-potential therapeutics of the post-antibiotic era. Adv Virus Res 83:143-216. http://dx.doi.org/10.1016/B978-0-12-394438-2.00005-0.
46. Carlton RM, Noordman WH, Biswas B, de Meester ED, Loessner MJ. 2005. Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul Toxicol Pharmacol 43:301-312. http://dx.doi.org/10.1016/j.yrtph.2005.08.005.
47. Gill JJ, Pacan JC, Carson ME, Leslie KE, Griffiths MW, Sabour PM. 2006. Efficacy and pharmacokinetics of bacteriophage therapy in treatment of subclinical Staphylococcus aureus mastitis in lactating dairy cattle. Antimicrob Agents Chemother 50:2912-2918. http://dx.doi.org/10.1128/AAC.01630-05.
48. Vandersteegen K, Kropinski AM, Nash JH, Noben JP, Hermans K, Lavigne R. 2013. Romulus and Remus, two phage isolates representing a distinct clade within the Twortlikevirus genus, display suitable properties for phage therapy applications. J Virol 87:3237-3247. http://dx.doi.org/10.1128/JVI.02763-12.
49. Klumpp J, Schmuki M, Sozhamannan S, Beyer W, Fouts DE, Bernbach V, Calendar R, Loessner MJ. 2014. The odd one out: Bacillus ACT bacteriophage CP-51 exhibits unusual properties compared to related Spounavirinae W.Ph. and Bastille. Virology 462-463C:299-308. http://dx.doi.org/10.1016/j.virol.2014.06.012.
50. Uchiyama J, Rashel M, Maeda Y, Takemura I, Sugihara S, Akechi K, Muraoka A, Wakiguchi H, Matsuzaki S. 2008. Isolation and characterization of a novel Enterococcus faecalis bacteriophage ϕEF24c as a therapeutic candidate. FEMS Microbiol Lett 278:200-206. http://dx.doi.org/10.1111/j.1574-6968.2007.00996.x.
51. Uchiyama J, Takemura I, Hayashi I, Matsuzaki S, Satoh M, Ujihara T, Murakami M, Imajoh M, Sugai M, Daibata M. 2011. Characterization of lytic enzyme open reading frame 9 (ORF9) derived from Enterococcus faecalis bacteriophage ϕEF24C. Appl Environ Microbiol 77:580-585. http://dx.doi.org/10.1128/AEM.01540-10.
52. Uchiyama J, Takemura I, Satoh M, Kato S, Ujihara T, Akechi K, Matsuzaki S, Daibata M. 2011. Improved adsorption of an Enterococcus faecalis bacteriophage ϕEF24C with a spontaneous point mutation. PLoS One 6:e26648. http://dx.doi.org/10.1371/journal.pone.0026648.
53. Mortensen DW, Boucher NE, Jr, Ryge G. 1965. A method of testing for marginal leakage of dental restorations with bacteria. J Dent Res 44:58-63. http://dx.doi.org/10.1177/00220345650440013101.
54. Knoll BM, Mylonakis E. 2014. Antibacterial bioagents based on principles of bacteriophage biology: an overview. Clin Infect Dis 58:528-534. http://dx.doi.org/10.1093/cid/cit771.