Biofilm-associated infections: Antibiotic resistance and novel therapeutic strategies

Future Microbiology

Volumn 8, Issue 7, 2013, Pages 877-886

  Sun, Fengjun ^a,b   Qu, Feng ^c   Ling, Yan ^d   Mao, Panyong ^c   Xia, Peiyuan ^a   Chen, Huipeng ^d   Zhou, Dongsheng ^b,c  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c BEIJING 302 HOSPITAL   (China)

^d BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

Author keywords

antibiotic resistance; biofilm; infection; treatment

Indexed keywords

ACETYLGLUCOSAMINIDASE; ALCOHOL; AMIKACIN; AMINOGLYCOSIDE ANTIBIOTIC AGENT; AMYLASE; ANTIBIOTIC AGENT; CEFOTAXIME; CELL DNA; CIPROFLOXACIN; DEOXYRIBONUCLEASE I; DNA; DNA BINDING PROTEIN; GENTAMICIN; GLUCAN; GLUCAN SYNTHASE; MULTIDRUG RESISTANCE PROTEIN; NATURAL PRODUCT; OXACILLIN; POLYPEPTIDE ANTIBIOTIC AGENT; QUINOLONE DERIVATIVE; RIFAMPICIN; TEICOPLANIN; TOBRAMYCIN; VANCOMYCIN;

ALCOHOL OXIDATION; AMINO ACID SEQUENCE; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTIFICIAL HEART PACEMAKER; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIOPHAGE; BIOFILM; BIOFILM ASSOCIATED INFECTION; CANDIDA ALBICANS; CELL AGGREGATION; CELL FUNCTION; CELL MEMBRANE; CENTRAL VENOUS CATHETER; CEREBROSPINAL FLUID SHUNTING; CONTACT LENS; DEVICE INFECTION; DNA DAMAGE; DNA REPAIR; DRUG DIFFUSION; DRUG EFFICACY; DRUG PENETRATION; ENDOTRACHEAL TUBE; EXTRACELLULAR MATRIX; FUNGAL STRAIN; GENE EXPRESSION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; JOINT PROSTHESIS; MECHANICAL HEART VALVE; NONHUMAN; PERITONEAL DIALYSIS CATHETER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW; STARVATION; STREPTOCOCCUS MUTANS; STRESS; TYPE VI SECRETION SYSTEM; ULTRASOUND; URINARY CATHETER;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL INFECTIONS; BACTERIAL PHYSIOLOGICAL PHENOMENA; BIOFILMS; DRUG RESISTANCE, BACTERIAL; HUMANS;

EID: 84880084458     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.13.58     Document Type: Review

References (84)

1. Flemming HC, Wingender J. The biofilm matrix. Nat. Rev. Microbiol. 8(9), 623-633 (2010).
2. Monds RD, O'Toole GA. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17(2), 73-87 (2009).
3. Stewart PS, Franklin MJ. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6(3), 199-210 (2008).
4. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 284(5418), 1318-1322 (1999).
5. Donlan RM. Biofilms and device-associated infections. Emerg. Infect. Dis. 7(2), 277-281 (2001).
6. Burmolle M, Thomsen TR, Fazli M et al. Biofilms in chronic infections-a matter of opportunity-monospecies biofilms in multispecies infections. FEMS Immunol. Med. Microbiol. 59(3), 324-336 (2010).
7. Romling U, Balsalobre C. Biofilm infections, their resilience to therapy and innovative treatment strategies. J. Intern. Med. 272(6), 541-561 (2012).
8. Douglas LJ. Candida biofilms and their role in infection. Trends Microbiol. 11(1), 30-36 (2003).
9. Wagner VE, Iglewski BH. P. aeruginosa biofilms in CF infection. Clin. Rev. Allergy Immunol. 35(3), 124-134 (2008).
10. Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35(4), 322-332 (2010).
11. Stewart PS. Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob. Agents Chemother. 40(11), 2517-2522 (1996).
12. Stewart PS, Davison WM, Steenbergen JN. Daptomycin rapidly penetrates a Staphylococcus epidermidis biofilm. Antimicrob. Agents Chemother. 53(8), 3505-3507 (2009).
13. Kumon H, Tomochika K, Matunaga T, Ogawa M, Ohmori H. A sandwich cup method for the penetration assay of antimicrobial agents through Pseudomonas exopolysaccharides. Microbiol. Immunol. 38(8), 615-619 (1994).
14. Shigeta M, Tanaka G, Komatsuzawa H, Sugai M, Suginaka H, Usui T. Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy 43(5), 340-345 (1997).
15. Singh R, Ray P, Das A, Sharma M. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. J. Antimicrob. Chemother. 65(9), 1955-1958 (2010).
16. Tanaka G, Shigeta M, Komatsuzawa H, Sugai M, Suginaka H, Usui T. Effect of the growth rate of Pseudomonas aeruginosa biofilms on the susceptibility to antimicrobial agents: b-lactams and fluoroquinolones. Chemotherapy 45(1), 28-36 (1999).
17. Mulcahy LR, Burns JL, Lory S, Lewis K. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J. Bacteriol. 192(23), 6191-6199 (2010).
18. Lafleur MD, Qi Q, Lewis K. Patients with long-term oral carriage harbor high-persister mutants of Candida albicans. Antimicrob. Agents Chemother. 54(1), 39-44 (2010).
19. Correia FF, D'Onofrio A, Rejtar T et al. Kinase activity of overexpressed HipA is required for growth arrest and multidrug tolerance in Escherichia coli. J. Bacteriol. 188(24), 8360-8367 (2006).
20. Nguyen D, Joshi-Datar A, Lepine F et al. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334(6058), 982-986 (2011).
21. Chatterji D, Ojha AK. Revisiting the stringent response, ppGpp and starvation signaling. Curr. Opin. Microbiol. 4(2), 160-165 (2001).
22. Michel B. After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol. 3(7), e255 (2005).
23. Beloin C, Valle J, Latour-Lambert P et al. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Microbiol. 51(3), 659-674 (2004).
24. Bernier SP, Lebeaux D, Defrancesco AS et al. Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genet. 9(1), e1003144 (2013).
25. Sadovskaya I, Vinogradov E, Li J, Hachani A, Kowalska K, Filloux A. High-level antibiotic resistance in Pseudomonas aeruginosa biofilm: the ndvB gene is involved in the production of highly glycerol-phosphorylated b-(1->3)-glucans, which bind aminoglycosides. Glycobiology 20(7), 895-904 (2010).
26. Nett JE, Sanchez H, Cain MT, Andes DR. Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J. Infect. Dis. 202(1), 171-175 (2010).
27. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O'Toole GA. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426(6964), 306-310 (2003).
28. Nett J, Lincoln L, Marchillo K et al. Putative role of b-1,3 glucans in Candida albicans biofilm resistance. Antimicrob. Agents Chemother. 51(2), 510-520 (2007).
29. Taff HT, Nett JE, Zarnowski R et al. A Candida biofilm-induced pathway for matrix glucan delivery: implications for drug resistance. PLoS Pathog. 8(8), e1002848 (2012).
30. Beaudoin T, Zhang L, Hinz AJ, Parr CJ, Mah TF. The biofilm-specific antibiotic resistance gene ndvB is important for expression of ethanol oxidation genes in Pseudomonas aeruginosa biofilms. J. Bacteriol. 194(12), 3128-3136 (2012).
31. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science 295(5559), 1487 (2002).
32. Mulcahy H, Charron-Mazenod L, Lewenza S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4(11), e1000213 (2008).
33. Rajendran R, Williams C, Lappin DF, Millington O, Martins M, Ramage G. Extracellular DNA release acts as an antifungal resistance mechanism in mature Aspergillus fumigatus biofilms. Eukaryot. Cell 12(3), 420-429 (2013).
34. Mima T, Sekiya H, Mizushima T, Kuroda T, Tsuchiya T. Gene cloning and properties of the RND-type multidrug efflux pumps MexPQ-OpmE and MexMN-OprM from Pseudomonas aeruginosa. Microbiol. Immunol. 49(11), 999-1002 (2005).
35. Zhang L, Mah TF. Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J. Bacteriol. 190(13), 4447-4452 (2008).
36. Lynch SV, Dixon L, Benoit MR et al. Role of the rapA gene in controlling antibiotic resistance of Escherichia coli biofilms. Antimicrob. Agents Chemother. 51(10), 3650-3658 (2007).
37. Coenye T, Van Acker H, Peeters E et al. Molecular mechanisms of chlorhexidine tolerance in Burkholderia cenocepacia biofilms. Antimicrob. Agents Chemother. 55(5), 1912-1919 (2011).
38. Rajendran R, Mowat E, Mcculloch E et al. Azole resistance of Aspergillus fumigatus biofilms is partly associated with efflux pump activity. Antimicrob. Agents Chemother. 55(5), 2092-2097 (2011).
39. Hood RD, Singh P, Hsu F et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7(1), 25-37 (2010).
40. Zhang L, Hinz AJ, Nadeau JP, Mah TF. Pseudomonas aeruginosa tssC1 links type VI secretion and biofilm-specific antibiotic resistance. J. Bacteriol. 193(19), 5510-5513 (2011).
41. Liao J, Sauer K. The MerR-like transcriptional regulator BrlR contributes to Pseudomonas aeruginosa biofilm tolerance. J. Bacteriol. 194(18), 4823-4836 (2012).
42. Mah TF. Regulating antibiotic tolerance within biofilm microcolonies. J. Bacteriol. 194(18), 4791-4792 (2012).
43. Martin-Yken H, Dagkessamanskaia A, Basmaji F, Lagorce A, Francois J. The interaction of Slt2 MAP kinase with Knr4 is necessary for signalling through the cell wall integrity pathway in Saccharomyces cerevisiae. Mol. Microbiol. 49(1), 23-35 (2003).
44. Nett JE, Sanchez H, Cain MT, Ross KM, Andes DR. Interface of Candida albicans biofilm matrix-associated drug resistance and cell wall integrity regulation. Eukaryot. Cell 10(12), 1660-1669 (2011).
45. Falagas ME, Kapaskelis AM, Kouranos VD, Kakisi OK, Athanassa Z, Karageorgopoulos DE. Outcome of antimicrobial therapy in documented biofilm-associated infections: a review of the available clinical evidence. Drugs 69(10), 1351-1361 (2009).
46. Jorge P, Lourenco A, Pereira MO. New trends in peptide-based anti-biofilm strategies: a review of recent achievements and bioinformatic approaches. Biofouling 28(10), 1033-1061 (2012).
47. Mai J, Tian XL, Gallant JW et al. A novel target-specific, salt-resistant antimicrobial peptide against the cariogenic pathogen Streptococcus mutans. Antimicrob. Agents Chemother. 55(11), 5205-5213 (2011).
48. Li LN, Guo LH, Lux R et al. Targeted antimicrobial therapy against Streptococcus mutans establishes protective non-cariogenic oral biofilms and reduces subsequent infection. Int. J. Oral Sci. 2(2), 66-73 (2010).
49. He J, Anderson MH, Shi W, Eckert R. Design and activity of a 'dual-targeted' antimicrobial peptide. Int. J. Antimicrob. Agents 33(6), 532-537 (2009).
50. Kaplan JB, Lovetri K, Cardona ST et al. Recombinant human DNase I decreases biofilm and increases antimicrobial susceptibility in staphylococci. J. Antibiot. (Tokyo) 65(2), 73-77 (2012).
51. Martins M, Henriques M, Lopez-Ribot JL, Oliveira R. Addition of DNase improves the in vitro activity of antifungal drugs against 0Candida albicans biofilms. Mycoses 55(1), 80-85 (2012).
52. Tetz GV, Artemenko NK, Tetz VV. Effect of DNase and antibiotics on biofilm characteristics. Antimicrob. Agents Chemother. 53(3), 1204-1209 (2009).
53. Kalpana BJ, Aarthy S, Pandian SK. Antibiofilm activity of a-amylase from Bacillus subtilis S8-18 against biofilm forming human bacterial pathogens. Appl. Biochem. Biotechnol. 167(6), 1778-1794 (2012).
54. Kaplan JB, Ragunath C, Ramasubbu N, Fine DH. Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous b-hexosaminidase activity. J. Bacteriol. 185(16), 4693-4698 (2003).
55. Darouiche RO, Mansouri MD, Gawande PV, Madhyastha S. Antimicrobial and antibiofilm efficacy of triclosan and DispersinB combination. J. Antimicrob. Chemother. 64(1), 88-93 (2009).
56. Donelli G, Francolini I, Romoli D et al. Synergistic activity of dispersin B and cefamandole nafate in inhibition of staphylococcal biofilm growth on polyurethanes. Antimicrob. Agents Chemother. 51(8), 2733-2740 (2007).
57. Izano EA, Wang H, Ragunath C, Ramasubbu N, Kaplan JB. Detachment and killing of Aggregatibacter actinomycetemcomitans biofilms by dispersin B and SDS. J. Dent. Res. 86(7), 618-622 (2007).
58. Burrowes B, Harper DR, Anderson J, Mcconville M, Enright MC. Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev. Anti Infect. Ther. 9(9), 775-785 (2011).
59. Donlan RM. Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol. 17(2), 66-72 (2009).
60. Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ. Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 67(6), 2746-2753 (2001).
61. Clark JR, March JB. Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol. 24(5), 212-218 (2006).
62. Briandet R, Lacroix-Gueu P, Renault M et al. Fluorescence correlation spectroscopy to study diffusion and reaction of bacteriophages inside biofilms. Appl. Environ. Microbiol. 74(7), 2135-2143 (2008).
63. Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob. Agents Chemother. 54(1), 397-404 (2010).
64. Kirby AE. Synergistic action of gentamicin and bacteriophage in a continuous culture population of Staphylococcus aureus. PLoS ONE 7(11), e51017 (2012).
65. Lu TK, Collins JJ. Dispersing biofilms with engineered enzymatic bacteriophage. Proc. Natl Acad. Sci. USA 104(27), 11197-11202 (2007).
66. Lu TK, Collins JJ. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc. Natl Acad. Sci. USA 106(12), 4629-4634 (2009).
67. Bartley J, Young D. Ultrasound as a treatment for chronic rhinosinusitis. Med. Hypotheses 73(1), 15-17 (2009).
68. Dong Y, Chen S, Wang Z, Peng N, Yu J. Synergy of ultrasound microbubbles and vancomycin against Staphylococcus epidermidis biofilm. J. Antimicrob. Chemother. 68(4), 816-826 (2013).
69. Carmen JC, Roeder BL, Nelson JL et al. Treatment of biofilm infections on implants with low-frequency ultrasound and antibiotics. Am. J. Infect. Control 33(2), 78-82 (2005).
70. Pitt WG, Ross SA. Ultrasound increases the rate of bacterial cell growth. Biotechnol. Prog. 19(3), 1038-1044 (2003).
71. Mayer CR, Geis NA, Katus HA, Bekeredjian R. Ultrasound targeted microbubble destruction for drug and gene delivery. Expert Opin. Drug Deliv. 5(10), 1121-1138 (2008).
72. He N, Hu J, Liu H et al. Enhancement of vancomycin activity against biofilms by using ultrasound-targeted microbubble destruction. Antimicrob. Agents Chemother. 55(11), 5331-5337 (2011).
73. Uroz S, Dessaux Y, Oger P. Quorum sensing and quorum quenching: the yin and yang of bacterial communication. Chembiochem 10(2), 205-216 (2009).
74. Kalia VC, Purohit HJ. Quenching the quorum sensing system: potential antibacterial drug targets. Crit. Rev. Microbiol. 37(2), 121-140 (2011).
75. Rasmussen TB, Bjarnsholt T, Skindersoe ME et al. Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J. Bacteriol. 187(5), 1799-1814 (2005).
76. Rasmussen TB, Givskov M. Quorum sensing inhibitors: a bargain of effects. Microbiology 152(Pt 4), 895-904 (2006).
77. Lonn-Stensrud J, Landin MA, Benneche T, Petersen FC, Scheie AA. Furanones, potential agents for preventing Staphylococcus epidermidis biofilm infections? J. Antimicrob. Chemother. 63(2), 309-316 (2009).
78. He Z, Wang Q, Hu Y et al. Use of the quorum sensing inhibitor furanone C-30 to interfere with biofilm formation by Streptococcus mutans and its luxS mutant strain. Int. J. Antimicrob. Agents 40(1), 30-35 (2012).
79. Francolini I, Norris P, Piozzi A, Donelli G, Stoodley P. Usnic acid, a natural antimicrobial agent able to inhibit bacterial biofilm formation on polymer surfaces. Antimicrob. Agents Chemother. 48(11), 4360-4365 (2004).
80. Pires RH, Lucarini R, Mendes-Giannini MJ. Effect of usnic acid on Candida orthopsilosis and C. parapsilosis. Antimicrob. Agents Chemother. 56(1), 595-597 (2012).
81. Brackman G, Cos P, Maes L, Nelis HJ, Coenye T. Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob. Agents Chemother. 55(6), 2655-2661 (2011).
82. Bakkiyaraj D, Pandian SK. In vitro and in vivo antibiofilm activity of a coral associated actinomycete against drug resistant Staphylococcus aureus biofilms. Biofouling 26(6), 711-717 (2010).
83. Bakkiyaraj D, Sivasankar C, Pandian SK. Inhibition of quorum sensing regulated biofilm formation in Serratia marcescens causing nosocomial infections. Bioorg. Med. Chem. Lett. 22(9), 3089-3094 (2012).
84. Nithya C, Devi MG, Karutha Pandian S. A novel compound from the marine bacterium Bacillus pumilus S6-15 inhibits biofilm formation in Gram-positive and Gram-negative species. Biofouling 27(5), 519-528 (2011).