Antibiotic-induced biofilm formation

International Journal of Artificial Organs

Volumn 34, Issue 9, 2011, Pages 737-751

  Kaplan, Jeffrey B ^a  

^a RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

c di GMP; Extracellular DNA; PNAG; ppGpp; Sub MIC; Subinhibitory

Indexed keywords

BIOFILMS; CELL SIGNALING;

BACTERIAL BIOFILM; BIOFILM FORMATION; C-DI-GMP; COLONIES OF BACTERIA; EXTRACELLULAR; EXTRACELLULAR DNA; PNAG; PPGPP; SUB-MIC; SUBINHIBITORY;

ANTIBIOTICS;

AMPICILLIN; ANTIBIOTIC AGENT; AZITHROMYCIN; CEFALEXIN; CEFALOTIN; CEFAMANDOLE; CEFAZOLIN; CEFOTAXIME; CEFTAZIDIME; CHLORAMPHENICOL; CIPROFLOXACIN; CLARITHROMYCIN; COTRIMOXAZOLE; DALFOPRISTIN PLUS QUINUPRISTIN; DAPTOMYCIN; ERYTHROMYCIN; GENTAMICIN; IMIPENEM; LINEZOLID; MOXIFLOXACIN; N ACETYLGLUCOSAMINE; NAFCILLIN; NOVOBIOCIN; OXACILLIN; PENICILLIN G; RIFAMPICIN; TETRACYCLINE; TIGECYCLINE; TOBRAMYCIN; VANCOMYCIN;

ACINETOBACTER BAUMANNII; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ANTIGENICITY; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; CELL ADHESION; CELL STRESS; CLOSTRIDIUM PERFRINGENS; CONCENTRATION RESPONSE; CYSTIC FIBROSIS; DEVICE INFECTION; DNA SYNTHESIS; ESCHERICHIA COLI; GENE CONTROL; GENE EXPRESSION; IN VITRO STUDY; INTRACELLULAR SIGNALING; LOW DRUG DOSE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METAGENOMICS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROTITER PLATE ASSAY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; RESPIRATORY FAILURE; REVIEW; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS LUGDUNENSIS; STREPTOCOCCUS INTERMEDIUS; TRANSPOSON;

EID: 81355136181     PISSN: 03913988     EISSN: None     Source Type: Journal    
DOI: 10.5301/ijao.5000027     Document Type: Review

References (86)

1. Mah TF, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 2001;9(1):34-39. Medline doi:10.1016/S0966-842X(00)01913-2
2. Singh R, Ray P, Das A, Sharma M. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Antimicrob Chemother. 2010;65(9):1955-1958. Medline doi:10.1093/jac/dkq257
3. Borriello G, Werner E, Roe F, et al. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob Agents Chemother. 2004;48(7):2659-2664. Medline doi:10.1128/AAC.48.7.2659-2664.2004
4. Lewis K. Persister cells. Annu Rev Microbiol. 2010;64:357-372. Medline doi:10.1146/annurev.micro.112408.134306
5. Neut D, van der Mei HC, Bulstra SK, Busscher HJ. The role of small-colony variants in failure to diagnose and treat biofilm infections in orthopedics. Acta Orthop. 2007;78(3):299-308. Medline doi:10.1080/17453670710013843
6. Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol. 2005;13(1):34-40. Medline doi:10.1016/j.tim.2004.11.010
7. Ichimiya T, Takeoka K, Hiramatsu K, et al. The influence of azithromycin on the biofilm formation of Pseudomonas aeruginosa in vitro. Chemotherapy. 1996;42(3):186-191. Medline doi:10.1159/000239440
8. Wagner T, Soong G, Sokol S, et al. Effects of azithromycin on clinical isolates of Pseudomonas aeruginosa from cystic fibrosis patients. Chest. 2005;128(2):912-919. Medline doi:10.1378/chest.128.2.912
9. Hoiby N. Antibiotic therapy for chronic infection of pseudomonas in the lung. Annu Rev Med. 1993;44:1-10. Medline doi:10.1146/annurev.me.44.020193.000245
10. Clement A, Tamalet A, Leroux E, et al. Long term effects of azithromycin in patients with cystic fibrosis: A double blind, placebo controlled trial. Thorax. 2006;61(10):895-902. Medline doi:10.1136/thx.2005.057950
11. Saiman L, Marshall BC, Mayer-Hamblett N, et al. Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA. 2003;290(13):1749-1756. Medline doi:10.1001/jama.290.13.1749
12. Favre-Bonte S, Kohler T, Van Delden C. Biofilm formation by Pseudomonas aeruginosa: role of the C4-HSL cell-tocell signal and inhibition by azithromycin. J Antimicrob Chemother. 2003;52(4):598-604. Medline doi:10.1093/jac/ dkg397
13. Nagino K, Kobayashi H. Influence of macrolides on mucoid alginate biosynthetic enzyme from Pseudomonas aeruginosa. Clin Microbiol Infect. 1997;3(4):432-439. Medline doi:10.1111/j.1469-0691.1997.tb00279.x
14. Tateda K, Comte R, Pechere JC, et al. Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2001;45(6):1930-1933. Medline doi:10.1128/AAC.45.6.1930-1933.2001
15. Odenholt I. Pharmacodynamic effects of subinhibitory antibiotic concentrations. Int J Antimicrob Agents. 2001;17(1):1-8. Medline doi:10.1016/S0924-8579(00)00243-0
16. Smith DL, Harris AD, Johnson JA, et al. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci USA. 2002;99(9):6434-6439. Medline doi:10.1073/pnas.082188899
17. Davies J, Spiegelman GB, Yim G. The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol. 2006;9(5):445-453. Medline doi:10.1016/j.mib.2006.08.006
18. Gardner AD. Morphological effects of penicillin on bacteria. Nature. 1940;146:837-838. doi:10.1038/146837b0
19. Washington JA. The effects and significance of subminimal inhibitory concentrations of antibiotics. Rev Infect Dis. 1979;1(5):781-786. Medline doi:10.1093/clinids/1.5.781
20. Lorian V. Medical relevance of low concentrations of antibiotics. J Antimicrob Chemother 1993; 31 Suppl D: 137-148. doi: 10.1093/jac/31.suppl_D.137
21. Gerber M, Walch C, Loffler B, et al. Effect of sub-MIC con centrations of metronidazole, vancomycin, clindamycin and linezolid on toxin gene transcription and production in Clostridium difficile. J Med Microbiol. 2008;57pt 6):776-783. Medline doi:10.1099/jmm.0.47739-0
22. Deneve C, Bouttier S, Dupuy B, et al. Effects of subinhibitory concentrations of antibiotics on colonization factor expression by moxifloxacin-susceptible and moxifloxacinresistant Clostridium difficile strains. Antimicrob Agents Chemother. 2009;53(12):5155-5162. Medline doi:10.1128/ AAC.00532-09
23. Stanton TB, Humphrey SB, Sharma VK, Zuerner RL. Collateral effects of antibiotics: carbadox and metronidazole induce VSH-1 and facilitate gene transfer among Brachyspira hyodysenteriae strains. Appl Environ Microbiol. 2008;74(10):2950-2956. Medline doi:10.1128/ AEM.00189-08
24. Goh EB, Yim G, Tsui W, et al. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc Natl Acad Sci USA. 2002;99(26):17025-17030. Medline doi:10.1073/pnas.252607699
25. Tsui WH, Yim G, Wang HH, et al. Dual effects of MLS antibiotics: transcriptional modulation and interactions on the ribosome. Chem Biol. 2004;11(9):1307-1316. Med line doi:10.1016/j.chembiol.2004.07.010
26. Yim G, de la Cruz F, Spiegelman GB, Davies J. Transcription modulation of Salmonella enterica serovar Typhimurium promoters by sub-MIC levels of rifampin. J Bacteriol. 2006;188(122):7988-7991. Medline doi:10.1128/ JB.00791-06
27. Weir EK, Martin LC, Poppe C, et al. Subinhibitory concentrations of tetracycline affect virulence gene expression in a multi-resistant Salmonella enterica subsp. enterica serovar Typhimurium DT104. Microbes Infect. 2008;10(8):901-907. Medline doi:10.1016/j.micinf.2008.05.005
28. Cummins J, Reen FJ, Baysse C, et al. Subinhibitory concentrations of the cationic antimicrobial peptide colistin induce the pseudomonas quinolone signal in Pseudomonas aeruginosa. Microbiology. 2009;155(Pt 9):2826-2837. Medline doi:10.1099/mic.0.025643-0
29. Lin JT, Connelly MB, Amolo C, et al. Global transcriptional response of Bacillus subtilis to treatment with subinhibitory concentrations of antibiotics that inhibit protein synthesis. Antimicrob Agents Chemother. 2005;49(5):1915-1926. Medline doi:10.1128/AAC.49.5.1915-1926.2005
30. Ng WL, Kazmierczak KM, Robertson GT, et al. Transcriptional regulation and signature patterns revealed by microarray analyses of Streptococcus pneumoniae R6 challenged with sublethal concentrations of translation inhibitors. J Bacteriol. 2003;185(1):359-370. Medline doi:10.1128/JB.185.1.359-370.2003
31. Linares JF, Gustafsson I, Baquero F, Martinez JL. Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA. 2006;103(51):19484-19489. Medline doi:10.1073/pnas.0608949103
32. Schadow KH, Simpson WA, Christensen GD. Characteristics of adherence to plastic tissue culture plates of coagulase-negative staphylococci exposed to subinhibitory concentrations of antimicrobial agents. J Infect Dis. 1988;157(1):71-77. Medline doi:10.1093/infdis/157.1.71
33. Hoffman LR, D'Argenio DA, MacCoss MJ, et al. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature. 2005;436(7054):1171-1175. Medline doi:10.1038/ nature03912
34. Bagge N, Schuster M, Hentzer M, et al. Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and beta-lactamase and alginate production. Antimicrob Agents Chemother. 2004;48(4):1175-1187. Medline doi:10.1128/AAC.48.4.1175-1187.2004
35. Boehm A, Steiner S, Zaehringer F, et al. Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol. 2009;72(6):1500-1516. Medline doi:10.1111/j.1365-2958.2009.06739.x
36. Ahmed NA, Petersen FC, Scheie AA. AI-2/LuxS is involved in increased biofilm formation by Streptococcus intermedius in the presence of antibiotics. Antimicrob Agents Chemother. 2009;53(10):4258-4263. Medline doi:10.1128/ AAC.00546-09
37. Wang Q, Sun FJ, Liu Y, et al. Enhancement of biofilm formation by subinhibitory concentrations of macrolides in icaADBC-positive and -negative clinical isolates of Staphylococcus epidermidis. Antimicrob Agents Chemother. 2010;54(6):2707-2711. Medline doi:10.1128/AAC.01565-09
38. Kaplan JB, Jabbouri S, Sadovskaya I. Extracellular DNAdependent biofilm formation by Staphylococcus epidermidis RP62A in response to subminimal inhibitory concentrations of antibiotics. Res Microbiol. 2011;162(5):525-541.
39. Perez-Giraldo C, Rodriguez-Benito A, Moran FJ, et al. Invitro slime production by Staphylococcus epidermidis in presence of subinhibitory concentrations of ciprofloxacin, ofloxacin and sparfloxacin. J Antimicrob Chemother. 1994;33(4):845-848. Medline doi:10.1093/jac/33.4.845
40. Majtan J, Majtanova L, Xu M, Majtan V. In vitro effect of subinhibitory concentrations of antibiotics on biofilm formation by clinical strains of Salmonella enterica serovar Typhimurium isolated in Slovakia. J Appl Microbiol. 2008;104(5):1294-1301. Medline doi:10.1111/j.1365-2672.2007.03653.x
41. Calabrese EJ, Baldwin LA. Hormesis: U-shaped dose responses and their centrality in toxicology. Trends Pharmacol Sci. 2001;22(6):285-291. Medline doi:10.1016/S0165-6147(00)01719-3
42. Kendig EL, Le HH, Belcher SM. Defining hormesis: evaluation of a complex concentration response phenomenon. Int J Toxicol. 2010;29(3):235-246. Medline doi:10.1177/1091581810363012
43. Haddadin RN, Saleh S, Al-Adham IS, et al. The effect of subminimal inhibitory concentrations of antibiotics on virulence factors expressed by Staphylococcus aureus biofilms. J Appl Microbiol. 2010;108(4):1281-1291. Medline doi:10.1111/j.1365-2672.2009.04529.x
44. Carsenti-Etesse H, Durant J, Entenza J, et al. Effects of subinhibitory concentrations of vancomycin and teicoplanin on adherence of staphylococci to tissue culture plates. Antimicrob Agents Chemother. 1993;37(4):921-923.
45. Cerca N, Martins S, Pier GB, et al. The relationship between inhibition of bacterial adhesion to a solid surface by sub-MICs of antibiotics and subsequent development of a biofilm. Res Microbiol. 2005;156(5-6):650-655. Medline doi:10.1016/j.resmic.2005.02.004
46. Polonio RE, Mermel LA, Paquette GE, Sperry JF. Eradication of biofilm-forming Staphylococcus epidermidis (RP62A) by a combination of sodium salicylate and vancomycin. Antimicrob Agents Chemother. 2001;45(11):3262-3266. Medline doi:10.1128/AAC.45.11.3262-3266.2001
47. Suman E, Jose S, D'Souza J, Kotian S. Does vancomycin inhibit biofilm production by coagulase-negative staphylococci? J Hosp Infect. 2009;73(1):86-87. Medline doi:10.1016/j.jhin.2009.06.001
48. Rupp ME, Hamer KE. Effect of subinhibitory concentrations of vancomycin, cefazolin, ofloxacin, L-ofloxacin and D-ofloxacin on adherence to intravascular catheters and biofilm formation by Staphylococcus epidermidis. J Antimicrob Chemother. 1998;41(2):155-161. Medline doi:10.1093/jac/41.2.155
49. Elliott D, Burns JL, Hoffman LR. Exploratory study of the prevalence and clinical significance of tobramycinmediated biofilm induction in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob Agents Chemother. 2010;54(7):3024-3026. Medline doi:10.1128/ AAC.00102-10
50. Mack D, Nedelmann M, Krokotsch A, et al. Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosaminecontaining polysaccharide intercellular adhesin. Infect Immun. 1994;62(8):3244-3253.
51. Vuong C, Kocianova S, Voyich JM, et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem. 2004;279(52):54881-54886. Medline doi:10.1074/jbc. M411374200
52. Vuong C, Voyich JM, Fischer ER, et al. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol. 2004;6(3):269-275. Medline doi:10.1046/j.1462-5822.2004.00367.x
53. Gerke C, Kraft A, Sussmuth R, et al. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epi- glucosedermidis polysaccharide intercellular adhesin. J Biol Chem. 1998;273(29):18586-18593. Medline doi:10.1074/ jbc.273.29.18586
54. Rachid S, Ohlsen K, Witte W, et al. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother. 2000;44(12):3357-3363. Medline doi:10.1128/ AAC.44.12.3357-3363.2000
55. Izano EA, Amarante MA, Kher WB, Kaplan JB. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol. 2008;74(2):470-476. Medline doi:10.1128/ AEM.02073-07
56. Qin Z, Ou Y, Yang L, et al. Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology. 2007;153(Pt 7):2083-2092. Medline doi:10.1099/mic.0.2007/006031-0
57. Hussain M, Herrmann M, von Eiff C, et al. A 140-kilodalton extracellular protein is essential for the accumulation of Staphylococcus epidermidis strains on surfaces. Infect Immun. 1997;65(2):519-524.
58. Sadovskaya I, Vinogradov E, Li J, Jabbouri S. Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr Res. 2004;339(8):1467-1473. Medline doi:10.1016/j.carres.2004.03.017
59. Holland LM, Conlon B, O'Gara JP. Mutation of tagO reveals an essential role for wall teichoic acids in Staphylococcus epidermidis biofilm development. Microbiology. 2011;157(Pt 2):408-418. Medline doi:10.1099/ mic.0.042234-0
60. Kuehl R, Al-Bataineh S, Gordon O, et al. Furanone at subinhibitory concentrations enhances staphylococcal biofilm formation by luxS repression. Antimicrob Agents Chemother. 2009;53(10):4159-4166. Medline doi:10.1128/ AAC.01704-08
61. Mirani ZA, Jamil N. Effect of sub-lethal doses of vancomycin and oxacillin on biofilm formation by vancomycin intermediate resistant Staphylococcus aureus. J Basic Microbiol. 2011;51(2):191-195. Medline doi:10.1002/ jobm.201000221
62. Bisognano C, Vaudaux PE, Lew DP, et al. Increased expression of fibronectin-binding proteins by fluoroquinoloneresistant Staphylococcus aureus exposed to subinhibitory levels of ciprofloxacin. Antimicrob Agents Chemother. 1997;41(5):906-913.
63. O'Neill E, Pozzi C, Houston P, et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin- binding proteins, FnBPA and FnBPB. J Bacteriol. 2008;190(11):3835-3850. Medline doi:10.1128/JB.00167-08
64. Subrt N, Mesak LR, Davies J. Modulation of virulence gene expression by cell wall active antibiotics in Staphylococ cus aureus. J Antimicrob Chemother. 2011;66(5):979-984. Medline doi:10.1093/jac/dkr043
65. Boles BR, Horswill AR. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 2008;4(4):e1000052. Medline doi:10.1371/journal.ppat.1000052
66. Frank KL, Reichert EJ, Piper KE, Patel R. In vitro effects of antimicrobial agents on planktonic and biofilm forms of Staphylococcus lugdunensis clinical isolates. Antimicrob Agents Chemother. 2007;51(3):888-895. Medline doi:10.1128/AAC.01052-06
67. Sailer FC, Meberg BM, Young KD. beta-Lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol Lett. 2003;226(2):245-249. Medline doi:10.1016/ S0378-1097(03)00616-5
68. Hanna A, Berg M, Stout V, Razatos A. Role of capsular colanic acid in adhesion of uropathogenic Escherichia coli. Appl Environ Microbiol. 2003;69(8):4474-4481. Medline doi:10.1128/AEM.69.8.4474-4481.2003
69. Bochner BR, Gadzinski P, Panomitros E. Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res. 2001;11(7):1246-1255. Medline doi:10.1101/gr.186501
70. Yildiz FH. Cyclic dimeric GMP signaling and regulation of surface-associated developmental programs. J Bacteriol. 2008;190(3):781-783. Medline doi:10.1128/JB.01852-07
71. Marr AK, Overhage J, Bains M, Hancock RE. The Lon protease of Pseudomonas aeruginosa is induced by aminoglycosides and is involved in biofilm formation and motility. Microbiology. 2007;153(Pt 2):474-482. Medline doi:10.1099/mic.0.2006/002519-0
72. Yasuda H, Ajiki Y, Koga T, et al. Interaction between biofilms formed by Pseudomonas aeruginosa and clarithromycin. Antimicrob Agents Chemother. 1993;37(9):1749-1755.
73. Gillis RJ, Iglewski BH. Azithromycin retards Pseudomonas aeruginosa biofilm formation. J Clin Microbiol. 2004;42(12):5842-5845. Medline doi:10.1128/ JCM.42.12.5842-5845.2004
74. Skindersoe ME, Alhede M, Phipps R, et al. Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2008;52(10):3648-3663. Medline doi:10.1128/AAC.01230-07
75. Vranes J. Effect of subminimal inhibitory concentrations of azithromycin on adherence of Pseudomonas aeruginosa to polystyrene. J Chemother. 2000;12(4):280-285.
76. Garey KW, Vo QP, Lewis RE, et al. Increased bacterial adherence and biomass in Pseudomonas aeruginosa bacteria exposed to clarithromycin. Diagn Microbiol Infect Dis. 2009;63(1):81-86. Medline doi:10.1016/j.diagmicrobio. 2008.09.007
77. Wozniak DJ, Keyser R. Effects of subinhibitory concentrations of macrolide antibiotics on Pseudomonas aeruginosa. Chest 2004; 125(2 Suppl): 62S-9S; quiz 69S.
78. Nucleo E, Steffanoni L, Fugazza G, et al. Growth in glucose- based medium and exposure to subinhibitory concentrations of imipenem induce biofilm formation in a multidrugresistant clinical isolate of Acinetobacter baumannii. BMC Microbiol. 2009;9:270. Medline doi:10.1186/1471-2180-9-270
79. Xavier KB, Bassler BL. LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol. 2003;6(2):191-197. Medline doi:10.1016/S1369-5274(03)00028-6
80. Ahmed NA, Petersen FC, Scheie AA. Biofilm formation and autoinducer-2 signaling in Streptococcus intermedius: role of thermal and pH factors. Oral Microbiol Immunol. 2008;23(6):492-497. Medline doi:10.1111/j.1399-302X.2008.00460.x
81. Fajardo A, Martinez JL. Antibiotics as signals that trigger specific bacterial responses. Curr Opin Microbiol. 2008;11(2):161-167. Medline doi:10.1016/j.mib.2008.02.006
82. Aminov RI. The role of antibiotics and antibiotic resistance in nature. Environ Microbiol. 2009;11(12):2970-2988. Medline doi:10.1111/j.1462-2920.2009.01972.x
83. Ratcliff WC, Denison RF. Microbiology. Alternative actions for antibiotics. Science. 2011;332(6029):547-548. Medline doi:10.1126/science.1205970
84. Bassler BL, Losick R. Bacterially speaking. Cell. 2006;125(2):237-246. Medline doi:10.1016/j.cell.2006.04.001
85. Dunne WM Jr. Effects of subinhibitory concentrations of vancomycin or cefamandole on biofilm production by coagulase- negative staphylococci. Antimicrob Agents Chemother. 1990;34(3):390-393.
86. Cargill JS, Upton M. Low concentrations of vancomycin stimulate biofilm formation in some clinical isolates of Staphylococcus epidermidis. J Clin Pathol. 2009;62(12):1112-1116. Medline doi:10.1136/jcp.2009.069021