Antibiotic resistance related to biofilm formation in Klebsiella pneumoniae

Pathogens

Volumn 3, Issue 3, 2014, Pages 743-758

  Vuotto, Claudia ^a,b   Longo, Francesca ^a   Balice, Maria Pia ^a   Donelli, Gianfranco ^a   Varaldo, Pietro E ^b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

Author keywords

Antibiotic resistance; Biofilm; Klebsiella pneumonia

Indexed keywords

AMIKACIN; AMPICILLIN; CARBAPENEM; CARBAPENEMASE; CEFEPIME; CEFOPERAZONE; CEFOTAXIME; CEFTAZIDIME; CEPHALOSPORIN; CHLORAMPHENICOL; CIPROFLOXACIN; EXTENDED SPECTRUM BETA LACTAMASE; GENTAMICIN; LIPOPOLYSACCHARIDE; MEROPENEM; METALLO BETA LACTAMASE; MONOBACTAM DERIVATIVE; NETILMICIN; OFLOXACIN; PIPERACILLIN; PIPERACILLIN PLUS TAZOBACTAM; TETRACYCLINE; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; BACTERIAL CAPSULE; BACTERIAL VIRULENCE; BACTERIUM PILUS; BIOFILM; CATHETER INFECTION; CONFOCAL LASER MICROSCOPY; DRUG EFFICACY; ESCHERICHIA COLI; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; FIMBRIA; HOSPITAL INFECTION; HUMAN; KLEBSIELLA PNEUMONIAE; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PLASMID; PSEUDOMONAS AERUGINOSA; REVIEW; TRANSMISSION ELECTRON MICROSCOPY; URINARY CATHETER;

KLEBSIELLA PNEUMONIAE; NEGIBACTERIA;

EID: 84943817547     PISSN: None     EISSN: 20760817     Source Type: Journal    
DOI: 10.3390/pathogens3030743     Document Type: Review

References (95)

1. Varaldo, P.E.; Biavasco, F.; Mannelli, S.; Pompei, R.; Proietti, A. Distribution and antibiotic susceptibility of extraintestinal clinical isolates of Klebsiella, Enterobacter and Serratia species. Eur. J. Clin. Microbiol. Infect. Dis. 1988, 4, 495–500.
2. Bagley, S.T. Habitat association of Klebsiella species. Infect. Control 1985, 6, 52–58.
3. Podschun, R.; Ullmann, U. Klebsiella spp. as nosocomial pathogens: Epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin. Microbiol. Rev. 1998, 11, 589–603.
4. Arakawa, Y.; Wacharotayankun, R.; Nagatsuka, T.; Ito, H.; Kato, N.; Ohta, M. Genomic organization of the Klebsiella pneumoniae cps region responsible for serotype K2 capsular polysaccharide synthesis in virulent strain Chedid. J. Bacteriol. 1995, 177, 1788–1796.
5. Gerlach, G.F.; Clegg, S.; Allen, B.L. Identification and characterization of the genes encoding the type 3 and type 1 fimbrial adhesins of Klebsiella pneumoniae. J. Clin. Microbiol. 1989, 171, 1262–1270.
6. Martino, P.D.; Bertin, Y.; Girardeau, J.P.; Livrelli, V.; Joly, B.; Darfeuille Michaud, A. Molecular characterization and adhesive properties of CF29K, and adhesion of Klebsiella pneumoniae strains involved in nosocomial infections. Infect. Immun. 1995, 63, 4336–4344.
7. Ørskov, I.; Ørskov, F. Serotyping of Klebsiella. Methods Microbiol. 1984, 14, 143–164.
8. Ehrenwort, L.; Baer, H. The pathogenicity of Klebsiella pneumoniae for mice: The relationship to the quantity and rate of production of type-specific capsular polysaccharide. J. Bacteriol. 1956, 72, 713–717.
9. Amako, K.; Meno, Y.; Takade, A. Fine structures of the capsules of Klebsiella pneumoniae and Escherichia coli K1. J. Bacteriol. 1988, 170, 4960–4962.
10. Podschun, R.; Ullmann, U. Klebsiella capsular type K7 in relation to toxicity, susceptibility to phagocytosis and resistance to serum. J. Med. Microbiol. 1992, 36, 250–254.
11. Williams, P.; Lambert, P.A.; Brown, M.R.W.; Jones, R.J. The role of the O and K antigens in determining the resistance of Klebsiella aerogenes to serum killing and phagocytosis. J. Gen. Microbiol. 1983, 129, 2181–2191.
12. Livrelli, V.; de Champs, C.; di Martino, P.; Darfeuille-Michaud, A.; Forestier, C.; Joly, B. Adhesive properties and antibiotic resistance of Klebsiella, Enterobacter, and Serratia clinical isolates involved in nosocomial infections. J. Clin. Microbiol. 1996, 34, 1963–1969.
13. Jones, G.W.; Isaacson, R.E. Proteinaceous bacterial adhesins and their receptors. Crit. Rev. Microbiol. 1983, 10, 229–260.
14. Ottow, J.C.G. Ecology, physiology, and genetics of fimbriae and pili. Annu. Rev. Microbiol. 1975, 29, 79–108.
15. Kline, K.A.; Dodson, K.W.; Caparon, M.G.; Hultgren, S.J. A tale of two pili: Assembly and function of pili in bacteria. Trends Microbiol. 2010, 18, 224–232.
16. Rosen, D.A.; Pinkner, J.S.; Jones, J.M.; Walker, J.N.; Clegg, S.; Hultgren, S.J. Utilization of an intracellular bacterial community pathway in Klebsiella pneumoniae urinary tract infection and the effects of FimK on type 1 pilus expression. Infect. Immun. 2008, 76, 3337–3345.
17. Struve, C.; Bojer, M.; Krogfelt, K.A. Characterization of Klebsiella pneumoniae type 1 fimbriae by detection of phase variation during colonization and infection and impact on virulence. Infect. Immun. 2008, 76, 4055–4065.
18. Alcántar-Curiel, M.D.; Blackburn, D.; Saldaña, Z.; Gayosso-Vázquez, C.; Iovine, N.M.; de la Cruz, M.A.; Girón, J.A. Multi-functional analysis of Klebsiella pneumoniae fimbrial types in adherence and biofilm formation. Virulence 2013, 4, 129–138.
19. Burmolle, M.; Bahl, M.I.; Jensen, L.B.; Sorensen, S.J.; Hansen, L.H. Type 3 fimbriae, encoded by the conjugative plasmid pOLA52, enhance biofilm formation and transfer frequencies in Enterobacteriaceae strains. Microbiology 2008, 154, 187–195.
20. Ong, C.L.; Ulett, G.C.; Mabbett, A.N.; Beatson, S.A.; Webb, R.I.; Monaghan, W.; Nimmo, G.R.; Looke, D.F.; McEwan, A.G.; Schembri, M.A. Identification of type 3 fimbriae in uropathogenic Escherichia coli reveals a role in biofilm formation. J. Bacteriol. 2008, 190, 1054–1063.
21. Ong, C.L.; Beatson, S.A.; Totsika, M.; Forestier, C.; McEwan, A.G.; Schembri, M.A. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol. 2010, 10, 183.
22. Lederman, E.R.; Crum, N.F. Pyogenic liver abscess with a focus on Klebsiella pneumoniae as a primary pathogen: An emerging disease with unique clinical characteristics. Am. J. Gastroenterol. 2005, 100, 322–331.
23. Fung, C.P.; Chang, F.Y.; Lee, S.C.; Hu, B.S.; Kuo, B.I.; Liu, C.Y.; Ho, M.; Siu, L.K. A global emerging disease of Klebsiella pneumoniae liver abscess: Is serotype K1 an important factor for complicated endophthalmitis? Gut 2002, 50, 420–424.
24. Laupland, K.B.; Ross, T.; Pitout, J.D.; Church, D.L.; Gregson, D.B. Community-onset urinary tract infections: A population-based assessment. Infection 2007, 35, 150–153.
25. Lin, W.H.; Kao, C.Y.; Yang, D.C.; Tseng, C.C.; Wu, A.B.; Teng, C.H.; Wang, M.C.; Wu, J.J. Clinical and microbiological characteristics of Klebsiella pneumoniae from community-acquired recurrent urinary tract infections. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 33, 1533–1539.
26. Tu, Y.C.; Lu, M.C.; Chiang, M.K.; Huang, S.P.; Peng, H.L.; Chang, H.Y.; Jan, M.S.; Lai, Y.C. Genetic requirements for Klebsiella pneumoniae-induced liver abscess in an oral infection model. Infect. Immun. 2009, 77, 2657–2671.
27. Kim, J.K.; Chung, D.R.; Wie, S.H.; Yoo, J.H.; Park, S.W. Risk factor analysis of invasive liver abscess caused by the K1 serotype Klebsiella pneumoniae. Eur. J. Clin. Microbiol. Infect. Dis. 2009, 28, 109–111.
28. Oelschlaeger, T.A.; Tall, B.D. Invasion of cultured human epithelial cells by Klebsiella pneumoniae isolated from the urinary tract. Infect. Immun. 1997, 6, 2950–2958.
29. Montgomerie, J.Z. Epidemiology of Klebsiella and hospital-associated infections. Rev. Infect. Dis. 1979, 1, 736–753.
30. Gupta, A. Hospital-acquired infections in the neonatal intensive care unit-Klebsiella pneumoniae. Semin. Perinatol. 2002, 26, 340–345.
31. Ko, W.C.; Paterson, D.L.; Sagnimeni, A.J.; Hansen, D.S.; von Gottberg, A.; Mohapatra, S.; Casellas, J.M.; Goossens, H.; Mulazimoglu, L.; Trenholme, G., et al. Community acquired Klebsiella pneumoniae bacteremia: Global differences in clinical patterns. Emerg. Infect. Dis. 2002, 8, 160–166.
32. Yinnon, A.M.; Butnaru, A.; Raveh, D.; Jerassy, Z.; Rudensky, B. Klebsiella bacteremia: community versus nosocomial infection. Mon. J. Assoc. Physicians 1996, 89, 933–941.
33. Niveditha, S.; Pramodhini, S.; Umadevi, S.; Kumar, S.; Stephen, S. The isolation and the biofilm formation of uropathogens in the patients with catheter associated urinary tract infections (UTIs). J. Clin. Diagn. Res. 2012, 6, 1478–1482.
34. Ronald, A. The etiology of urinary tract infection: Traditional and emerging pathogens. Am. J. Med. 2002, 113, 14S–19S.
35. Frank, D.N.; Wilson, S.S.; St Amand, A.L.; Pace, N.R. Culture independent microbiological analysis of Foley urinary catheter biofilms. PLoS One 2009, 4, e7811.
36. Lye, W.C.; Chan, R.K.T.; Lee, E.J.C.; Kumarasinghe, G. Urinary tract infections in patients with diabetes mellitus. J. Infect. 1992, 24, 169–174.
37. Bennett, C.J.; Young, M.N.; Darrington, H. Differences in urinary tract infection in male and female spinal cord injury patients on intermittent catheterization. Paraplegia 1995, 33, 69–72.
38. Siegman-Igra, Y.; Golan, H.; Schwartz, D.; Cahaner, Y.; de-Mayo, G.; Orni-Wasserlauf, R. Epidemiology of vascular catheter-related bloodstream infections in a large university hospital in Israel. Scand. J. Infect. Dis. 2000, 32, 411–415.
39. Singhai, M.; Malik, A.; Shahid, M.; Malik, M.A.; Goyal, R. A study on device-related infections with special reference to biofilm production and antibiotic resistance. J. Glob. Infect. Dis. 2012, 4, 193–198.
40. Lin, M.Y.; Lyles-Banks, R.D.; Lolans, K.; Hines, D.W.; Spear, J.B.; Petrak, R.; Trick, W.E.; Weinstein, R.A.; Hayden, M.K.; Centers for Disease Control and Prevention Epicenters Program. The importance of long-term acute care hospitals in the regional epidemiology of Klebsiella pneumoniae carbapenemase-producing Enterobacteriaceae. Clin. Infect. Dis. 2013, 57, 1246–1252.
41. Orsi, G.B.; Scorzolini, L.; Franchi, C.; Mondillo, V.; Rosa, G.; Venditti, M. Hospital-acquired infection surveillance in a neurosurgical intensive care unit. J. Hosp. Infect. 2006, 64, 23–29.
42. Giani, T.; Pini, B.; Arena, F.; Conte, V.; Bracco, S.; Migliavacca, R.; AMCLI-CRE Survey Participants; Pantosti, A.; Pagani, L.; Luzzaro, F., et al. Epidemic diffusion of KPC carbapenemase-producing Klebsiella pneumoniae in Italy: Results of the first countrywide survey, 15 May to 30 June 2011. Euro Surveill. 2013, 30, 18–22.
43. Azzopardi, E.A.; Azzopardi, E.; Camilleri, L.; Villapalos, J.; Boyce, D.E.; Dziewulski, P.; Dickson, W.A.; Whitaker, I.S. Gram negative wound infection in hospitalised adult burn patients-systematic review and metanalysis. PLoS One 2014, 9, e95042.
44. Varaldo, P.E.; Nicoletti, G.; Schito, G.C.; Maida, A.; Facinelli, B.; Stefani, S.; Gianrossi, G.; Muresu, E. Circulation in Italy of beta-lactamase-producing strains within the major groups of bacterial pathogens. Eur. J. Epidemiol. 1990, 6, 287–292.
45. Guérillot, F.; Carret, G.; Flandrois, J.P. A statistical evaluation of the bactericidal effects of ceftibuten in combination with aminoglycosides and ciprofloxacin. J. Antimicrob. Chemother. 1993, 32, 685–694.
46. Elkhaïli, H.; Kamili, N.; Linger, L.; Levêque, D.; Pompei, D.; Monteil, H.; Jehl, F. In vitro time-kill curves of cefepime and cefpirome combined with amikacin, gentamicin or ciprofloxacin against Klebsiella pneumoniae producing extended-spectrum beta-lactamase. Chemotherapy 1997, 43, 245–253.
47. Traub, W.H.; Schwarze, I.; Bauer, D. Nosocomial outbreak of cross-infection due to multiple-antibiotic-resistant Klebsiella pneumoniae: Characterization of the strain and antibiotic susceptibility studies. Chemotherapy 2000, 46, 1–14.
48. Patel, G.; Bonomo, R.A. Status report on carbapenemases: Challenges and prospects. Expert Rev. Anti Infect. Ther. 2011, 9, 555–570.
49. Voulgari, E.; Poulou, A.; Koumaki, V.; Tsakris, A. Carbapenemase-producing Enterobacteriaceae: Now that the storm is finally here, how will timely detection help us fight back? Future Microbiol. 2013, 8, 27–39.
50. Yigit, H.; Queenan, A.M.; Anderson, G.J.; Domenech-Sanchez, A.; Biddle, J.W.; Steward, C.D.; Alberti, S.; Bush, K.; Tenover, F.C. Novel carbapenem-hydrolyzing beta-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob. Agents Chemother. 2001, 45, 1151–1161.
51. Papp-Wallace, K.M.; Bethel, C.R.; Distler, A.M.; Kasuboski, C.; Taracila, M.; Bonomo, R.A. Inhibitor resistance in the KPC-2 beta-lactamase, a preeminent property of this class A beta-lactamase. Antimicrob. Agents Chemother. 2010, 54, 890–897.
52. Molton, J.S.; Tambyah, P.A.; Ang, B.S.; Ling, M.L.; Fisher, D.A. The global spread of healthcare-associated multidrug-resistant bacteria: A perspective from Asia. Clin. Infect. Dis. 2013, 56, 1310–1318.
53. Grundmann, H.; Livermore, D.M.; Giske, C.G.; Canton, R.; Rossolini, G.M.; Campos, J.; Vatopoulos, A.; Gniadkowski, M.; Toth, A.; Pfeifer, Y., et al. CNSE Working Group. Carbapenem-non-susceptible Enterobacteriaceae in Europe: Conclusions from a meeting of national experts. Euro Surveill. 2010, 15, 19711.
54. Miriagou, V.; Cornaglia, G.; Edelstein, M.; Galani, I.; Giske, C.G.; Gniadkowski, M.; Malamou-Lada, E.; Martinez-Martinez, L.; Navarro, F.; Nordmann, P., et al. Acquired carbapenemases in Gram-negative bacterial pathogens: Detection and surveillance issues. Clin. Microbiol. Infect. 2010, 16, 112–122.
55. Tzouvelekis, L.S.; Markogiannakis, A.; Psichogiou, M.; Tassios, P.T.; Daikos, G.L. Carbapenemases in Klebsiella pneumoniae and other Enterobacteriaceae: An evolving crisis of global dimensions. Clin. Microbiol. Rev. 2012, 25, 682–707.
56. Wang, Q.; Li, B.; Tsang, A.K.; Yi, Y.; Woo, P.C.; Liu, C.H. Genotypic analysis of Klebsiella pneumoniae isolates in a Beijing Hospital reveals high genetic diversity and clonal population structure of drug-resistant isolates. PLoS One 2013, 8, e57091.
57. Le Chevallier, M.W.; Cawthon, C.D.; Lee, R.G. Factors promoting survival of bacteria in chlorinated water supplies. Appl. Environ. Microbiol. 1988, 54, 649–654.
58. Reid, G.; Charbonneau-Smith, R.; Lam, D.; Kang, Y.S.; Lacerte, M.; Hayes, K.C. Bacterial biofilm formation in the urinary bladder of spinal cord injured patients. Paraplegia 1992, 30, 711–717.
59. Yang, D.; Zhang, Z. Biofilm-forming Klebsiella pneumoniae strains have greater likelihood of producing extended-spectrum beta-lactamases. J. Hosp. Infect. 2008, 68, 369–371.
60. Nicolau Korres, A.M.; Aquije, G.M.; Buss, D.S.; Ventura, J.A.; Fernandes, P.M.; Fernandes, A.A. Comparison of biofilm and attachment mechanisms of a phytopathological and clinical isolate of Klebsiella pneumoniae subsp. pneumoniae. Sci. World J. 2013, 10, 925375.
61. Donelli, G.; Vuotto, C. Biofilm-based infections in long-term care facilities. Future Microbiol. 2014, 9, 175–188.
62. Langstraat, J.; Bohse, M.; Clegg, S. Type 3 fimbrial shaft (MrkA) of Klebsiella pneumoniae, but not the fimbrial adhesin (MrkD), facilitates biofilm formation. Infect. Immun. 2001, 69, 5805–5812.
63. Di Martino, P.; Cafferini, N.; Joly, B.; Darfeuille-Michaud, A. Klebsiella pneumoniae type 3 pili facilitate adherence and biofilm formation on abiotic surfaces. Res. Microbiol. 2003, 154, 9–16.
64. Jagnow, J.; Clegg, S. Klebsiella pneumoniae MrkD-mediated biofilm formation on extracellular matrix- and collagen-coated surfaces. Microbiology 2003, 149, 2397–2405.
65. Lavender, H.F.; Jagnow, J.R.; Clegg, S. Biofilm formation in vitro and virulence in vivo of mutants of Klebsiella pneumoniae. Infect. Immun. 2004, 72, 4888–4890.
66. Boddicker, J.D.; Anderson, R.A.; Jagnow, J.; Clegg, S. Signature-tagged mutagenesis of Klebsiella pneumoniae to identify genes that influence biofilm formation on extracellular matrix material. Infect. Immun. 2006, 74, 4590–4597.
67. Schroll, C.; Barken, K.B.; Krogfelt, K.A.; Struve, C. Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation. BMC Microbiol. 2010, 10, 179.
68. Johnson, J.G.; Clegg, S. Role of MrkJ, a phosphodiesterase, in type 3 fimbrial expression and biofilm formation in Klebsiella pneumoniae. J. Bacteriol. 2010, 192, 3944–3950.
69. Murphy, C.N.; Mortensen, M.S.; Krogfelt, K.A.; Clegg, S. Role of Klebsiella pneumoniae type 1 and type 3 fimbriae in colonizing silicone tubes implanted into the bladders of mice as a model of catheter-associated urinary tract infections. Infect. Immun. 2013, 81, 3009–3017.
70. Balestrino, D.; Ghigo, J.M.; Charbonnel, N.; Haagensen, J.A.; Forestier, C. The characterization of functions involved in the establishment and maturation of Klebsiella pneumoniae in vitro biofilm reveals dual roles for surface exopolysaccharides. Environ. Microbiol. 2008, 10, 685–701.
71. Wu, M.C.; Lin, T.L.; Hsieh, P.F.; Yang, H.C.; Wang, J.T. Isolation of genes involved in biofilm formation of a Klebsiella pneumoniae strain causing pyogenic liver abscess. PLoS One 2011, 6, e23500.
72. Huang, T.W.; Lam, I.; Chang, H.Y.; Tsai, S.F.; Palsson, B.O.; Charusanti, P. Capsule deletion via a λ-Red knockout system perturbs biofilm formation and fimbriae expression in Klebsiella pneumoniae MGH 78578. BMC Res. Notes 2014, 8, 7–13.
73. Siebel, M.A.; Characklis, W.G. Observations of binary population biofilms. Biotechnol. Bioeng. 1991, 37, 778–789.
74. Skillman, L.C.; Sutherland, I.W.; Jones, M.V. The role of exopolysaccharides in dual species biofilm development. J. Appl. Microbiol. 1998, 85, 13S–18S.
75. Stickler, D.; Morris, N.; Moreno, M.C.; Sabbuba, N. Studies on the formation of crystalline bacterial biofilms on urethral catheters. Eur. J. Clin. Microbiol. Infect. Dis. 1998, 17, 649–652.
76. Macleod, S.M.; Stickler, D.J. Species interactions in mixed-community crystalline biofilms on urinary catheters. J. Med. Microbiol. 2007, 56, 1549–1557.
77. Lee, K.W.; Periasamy, S.; Mukherjee, M.; Xie, C.; Kjelleberg, S.; Rice, S.A. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. 2014, 8, 894–907.
78. Chen, B.M.; Yu, J.L.; Liu, G.X.; Hu, L.Y.; Li, L.Q.; Li, F.; Yang, H. Electron microscopic analysis of biofilm on tracheal tubes removed from intubated neonates and the relationship between bilofilm and lower respiratory infection. Zhonghua Er Ke Za Zhi. 2007, 45, 655–660.
79. Anderl, J.N.; Franklin, M.J.; Stewart, P.S. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 2000, 44, 1818–1824.
80. Zahller, J.; Stewart, P.S. A transmission electron microscopic study of antibiotic action on Klebsiella pneumoniae biofilm. Antimicrob. Agents Chemother. 2002, 46, 2679–2683.
81. Anderl, J.N.; Zahller, J.; Roe, F.; Stewart, P.S. Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 2003, 47, 1251–1256.
82. Cernohorská, L.; Votava, M. Determination of minimal regrowth concentration (MRC) in clinical isolates of various biofilm-forming bacteria. Folia Microbiol. (Praha) 2004, 49, 75–78.
83. Liaqat, I.; Sumbal, F.; Sabri, A.N. Tetracycline and chloramphenicol efficiency against selected biofilm forming bacteria. Curr. Microbiol. 2009, 59, 212–220.
84. Fonseca, A.P.; Extremina, C.; Fonseca, A.F.; Sousa, J.C. Effect of subinhibitory concentration of piperacillin/tazobactam on Pseudomonas aeruginosa. J. Med. Microbiol. 2004, 53, 903–910.
85. Rachid, S.; Ohlsen, K.; Witte, W.; Hacker, J.; Ziebuhr, W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesion expression in biofilm forming Staphylococcus epidermidis. Antimicrob. Agents Chemother. 2000, 44, 3357–3363.
86. Singla, S.; Harjai, K.; Chhibber, S. Susceptibility of different phases of biofilm of Klebsiella pneumoniae to three different antibiotics. J. Antibiot. (Tokyo) 2013, 66, 61–66.
87. Bellifa, S.; Hassaine, H.; Balestrino, D.; Charbonnel, N.; M’hamedi, I.; Terki, I.K.; Lachachi, M.; Didi, W.; Forestier, C. Evaluation of biofilm formation of K. pneumoniae isolated from medical devices at the University Hospital of Tlemcen, Algeria. Afr. J. Microbiol. Res. 2013, 7, 5558–5564.
88. Naparstek, L.; Carmeli, Y.; Navon-Venezia, S.; Banin, E. Biofilm formation and susceptibility to gentamicin and colistin of extremely drug-resistant KPC-producing Klebsiella pneumoniae. J. Antimicrob. Chemother. 2014, 69, 1027–1034.
89. Singla, S.; Harjai, K.; Chhibber, S. Artificial Klebsiella pneumoniae biofilm model mimicking in vivo system: Altered morphological characteristics and antibiotic resistance. J. Antibiot. (Tokyo) 2014, 67, 305–309.
90. Chen, P.; Seth, A.K.; Abercrombie, J.J.; Mustoe, T.A.; Leung, K.P. Activity of imipenem against Klebsiella pneumoniae biofilms in vitro and in vivo. Antimicrob. Agents Chemother. 2014, 58, 1208–1213.
91. Fuursted, K.; Schøler, L.; Hansen, F.; Dam, K.; Bojer, M.S.; Hammerum, A.M.; Dagnæs-Hansen, F.; Olsen, A.; Jasemian, Y.; Struve, C. Virulence of a Klebsiella pneumoniae strain carrying the New Delhi metallo-beta-lactamase-1 (NDM-1). Microbes Infect. 2012, 14, 155–158.
92. Subramanian, P.; Shanmugam, N.; Sivaraman, U.; Kumar, S.; Selvaraj, S. Antiobiotic resistance pattern of biofilm-forming uropathogens isolated from catheterized patients in Pondicherry, India. Australas. Med. J. 2012, 5, 344–348.
93. Sanchez, C.J., Jr.; Mende, K.; Beckius, M.L.; Akers, K.S.; Romano, D.R.; Wenke, J.C.; Murray, C.K. Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect. Dis. 2013, 29, 13–47.
94. Hennequin, C.; Aumeran, C.; Robin, F.; Traore, O.; Forestier, C. Antibiotic resistance and plasmid transfer capacity in biofilm formed with a CTX-M-15-producing Klebsiella pneumoniae isolate. J. Antimicrob. Chemother. 2012, 67, 2123–2130.
95. Hennequin, C.; Robin, F.; Cabrolier, N.; Bonnet, R.; Forestier, C. Characterization of a DHA-1-producing Klebsiella pneumoniae strain involved in an outbreak and role of the AmpR regulator in virulence. Antimicrob. Agents Chemother. 2012, 56, 288–294