Klebsiella pneumoniae Biofilms and Their Role in Disease Pathogenesis

Abstract

The ability to form biofilms is a crucial virulence trait for several microorganisms, including Klebsiella pneumoniae – a Gram-negative encapsulated bacterium often associated with nosocomial infections. It is estimated that 65-80% of bacterial infections are biofilm related. Biofilms are complex bacterial communities composed of one or more species encased in an extracellular matrix made of proteins, carbohydrates and genetic material derived from the bacteria themselves as well as from the host. Bacteria in the biofilm are shielded from immune responses and antibiotics. The present review discusses the characteristics of K. pneumoniae biofilms, factors affecting biofilm development, and their contribution to infections. We also explore different model systems designed to study biofilm formation in this species. A great number of factors contribute to biofilm establishment and maintenance in K. pneumoniae , which highlights the importance of this mechanism for the bacterial fitness. Some of these molecules could be used in future vaccines against this bacterium. However, there is still a lack of in vivo models to evaluate the contribution of biofilm development to disease pathogenesis. With that in mind, the combination of different methodologies has great potential to provide a more detailed scenario that more accurately reflects the steps and progression of natural infection.

References 120

1. 1.

   Abraham W. R. (2016 ). Going Beyond the Control of Quorum-Sensing to Combat Biofilm Infections. Antibiot. (Basel). 5 (1), 1–16

   Not in our library10.3390/antibiotics5010003

2. 2.

   Abraham J. M. Freitag C. S. Clements J. R. Eisenstein B. I. (1985 ). An Invertible Element of DNA Controls Phase Variation of Type 1 Fimbriae of Escherichia Coli. Proc. Natl. Acad. Sci. U.S.A. 82 (17), 5724–5727

   Not in our library10.1073/pnas.82.17.5724

3. 3.

   Alcantar-Curiel M. D. Blackburn D. Saldana Z. Gayosso-Vazquez C. Iovine N. M. de la Cruz M. A.. (2013 ). Multi-Functional Analysis of Klebsiella Pneumoniae Fimbrial Types in Adherence and Biofilm Formation. Virulence 4 (2), 129–138

   Not in our library10.4161/viru.22974

4. 4.

   Ares M. A. Fernandez-Vazquez J. L. Rosales-Reyes R. Jarillo-Quijada M. D. von Bargen K. Torres J.. (2016 ). H-NS Nucleoid Protein Controls Virulence Features of Klebsiella Pneumoniae by Regulating the Expression of Type 3 Pili and the Capsule Polysaccharide. Front. Cell Infect. Microbiol. 6, 13

   Not in our library10.3389/fcimb.2016.00013

5. 5.

   Assoni L. Girardello R. Converso T. R. Darrieux M. (2021 ). Current Stage in the Development of Klebsiella Pneumoniae Vaccines. Infect. Dis. Ther. 10 (4), 2157–2175

   Not in our library10.1007/s40121-021-00533-4

6. 6.

   Attinger C. Wolcott R. (2012 ). Clinically Addressing Biofilm in Chronic Wounds. Adv. Wound Care (New. Rochelle). 1 (3), 127–132

   Not in our library10.1089/wound.2011.0333

7. 7.

   Babu L. Uppalapati S. R. Sripathy M. H. Reddy P. N. (2017 ). Evaluation of Recombinant Multi-Epitope Outer Membrane Protein-Based Klebsiella Pneumoniae Subunit Vaccine in Mouse Model. Front. Microbiol. 8, 1805

   Not in our library10.3389/fmicb.2017.01805

8. 8.

   Balestrino D. Ghigo J. M. Charbonnel N. Haagensen J. A. Forestier C. (2008 ). The Characterization of Functions Involved in the Establishment and Maturation of Klebsiella Pneumoniae In Vitro Biofilm Reveals Dual Roles for Surface Exopolysaccharides. Environ. Microbiol. 10 (3), 685–701

   Not in our library10.1111/j.1462-2920.2007.01491.x

9. 9.

   Balestrino D. Haagensen J. A. Rich C. Forestier C. (2005 ). Characterization of Type 2 Quorum Sensing in Klebsiella Pneumoniae and Relationship With Biofilm Formation. J. Bacteriol. 187 (8), 2870–2880

   Not in our library10.1128/jb.187.8.2870-2880.2005

10. 10.

    Barnard A. M. Bowden S. D. Burr T. Coulthurst S. J. Monson R. E. Salmond G. P. (2007 ). Quorum Sensing, Virulence and Secondary Metabolite Production in Plant Soft-Rotting Bacteria. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362 (1483), 1165–1183

    Not in our library10.1098/rstb.2007.2042

11. 11.

    Baselga R. Albizu I. Amorena B. (1994 ). Staphylococcus Aureus Capsule and Slime as Virulence Factors in Ruminant Mastitis. A. Rev. Vet. Microbiol. 39 (3-4), 195–204

    Not in our library10.1016/0378-1135(94)90157-0

12. 12.
    Klebsiella pneumoniae infection biology: living to counteract host defences · 2018

    No notice
13. 13.

    Benthall G. Touzel R. E. Hind C. K. Titball R. W. Sutton J. M. Thomas R. J.. (2015 ). Evaluation of Antibiotic Efficacy Against Infections Caused by Planktonic or Biofilm Cultures of Pseudomonas Aeruginosa and Klebsiella Pneumoniae in Galleria Mellonella. Int. J. Antimicrob. Agents 46 (5), 538–545

    Not in our library10.1016/j.ijantimicag.2015.07.014

14. 14.
    Starvation, Together with the SOS Response, Mediates High Biofilm-Specific Tolerance to the Fluoroquinolone Ofloxacin · 2013

    No notice
15. 15.

    Bjarnsholt T. Alhede M. Alhede M. Eickhardt-Sorensen S. R. Moser C. Kuhl M.. (2013 ). The In Vivo Biofilm. Trends Microbiol. 21 (9), 466–474

    Not in our library10.1016/j.tim.2013.06.002

16. 16.

    Booth S. C. Rice S. A. (2020 ). Influence of Interspecies Interactions on the Spatial Organization of Dual Species Bacterial Communities. Biofilm 2, 100035

    Not in our library10.1016/j.bioflm.2020.100035

17. 17.

    Bowen W. H. Burne R. A. Wu H. Koo H. (2018 ). Oral Biofilms: Pathogens, Matrix, and Polymicrobial Interactions in Microenvironments. Trends Microbiol. 26 (3), 229–242

    Not in our library10.1016/j.tim.2017.09.008

18. 18.

    Brindhadevi K. LewisOscar F. Mylonakis E. Shanmugam S. Verma T. N. Pugazhendhi A. (2020 ). Biofilm and Quorum Sensing Mediated Pathogenicity in Pseudomonas Aeruginosa. Process. Biochem. 96, 49–57

    Not in our library10.1016/j.procbio.2020.06.001

19. 19.

    Bronesky D. Wu Z. Marzi S. Walter P. Geissmann T. Moreau K.. (2016 ). Staphylococcus Aureus RNAIII and Its Regulon Link Quorum Sensing, Stress Responses, Metabolic Adaptation, and Regulation of Virulence Gene Expression. Annu. Rev. Microbiol. 70, 299–316

    Not in our library10.1146/annurev-micro-102215-095708

20. 20.

    Bruchmann S. Feltwell T. Parkhill J. Short F. L. (2021 ). Identifying Virulence Determinants of Multidrug-Resistant Klebsiella Pneumoniae in Galleria Mellonella. Pathog. Dis. 79 (3), 1–15

    Not in our library10.1093/femspd/ftab009

21. 21.

    Buffet A. Rocha E.P.C Rendueles O. (2021 ). Nutrient conditions are primary drivers of bacterial capsule maintenance in Klebsiella. Proc Biol Sci. 288 (1946), 20202876

    Not in our library10.1098/rspb.2020.2876

22. 22.
    Streptococcus pneumoniae biofilm formation and dispersion during colonization and disease · 2015

    No notice
23. 23.

    Chatterjee S. Maiti P. Dey R. Kundu A. Dey R. (2014 ). Biofilms on Indwelling Urologic Devices: Microbes and Antimicrobial Management Prospect. Ann. Med. Health Sci. Res. 4 (1), 100–104

    Not in our library10.4103/2141-9248.126612

24. 24.

    Chen L. Wilksch J. J. Liu H. Zhang X. Torres V. V. L. Bi W.. (2020 ). Investigation of LuxS-Mediated Quorum Sensing in Klebsiella Pneumoniae. J. Med. Microbiol. 69 (3), 402–413

    Not in our library10.1099/jmm.0.001148

25. 25.

    Chew K. L. Lin R. T. P. Teo J. W. P. (2017 ). Klebsiella Pneumoniae in Singapore: Hypervirulent Infections and the Carbapenemase Threat. Front. Cell Infect. Microbiol. 7, 515

    Not in our library10.3389/fcimb.2017.00515

26. 26.

    Chhibber S. Nag D. Bansal S. (2013 ). Inhibiting Biofilm Formation by Klebsiella Pneumoniae B5055 Using an Iron Antagonizing Molecule and a Bacteriophage. BMC Microbiol. 13, 174

    Not in our library10.1186/1471-2180-13-174

27. 27.

    Cubero M. Marti S. Dominguez M. A. Gonzalez-Diaz A. Berbel D. Ardanuy C. (2019 ). Hypervirulent Klebsiella Pneumoniae Serotype K1 Clinical Isolates Form Robust Biofilms at the Air-Liquid Interface. PloS One 14 (9), e0222628

    Not in our library10.1371/journal.pone.0222628

28. 28.

    Dao T. T. Liebenthal D. Tran T. K. Ngoc Thi Vu B. Ngoc Thi Nguyen D. Thi Tran H. K.. (2014 ). Klebsiella Pneumoniae Oropharyngeal Carriage in Rural and Urban Vietnam and the Effect of Alcohol Consumption. PloS One 9 (3), e91999

    Not in our library10.1371/journal.pone.0091999

29. 29.

    De Araujo C. Balestrino D. Roth L. Charbonnel N. Forestier C. (2010 ). Quorum Sensing Affects Biofilm Formation Through Lipopolysaccharide Synthesis in Klebsiella Pneumoniae. Res. Microbiol. 161 (7), 595–603

    Not in our library10.1016/j.resmic.2010.05.014

30. 30.

    Desai S. Sanghrajka K. Gajjar D. (2019 ). High Adhesion and Increased Cell Death Contribute to Strong Biofilm Formation in Klebsiella Pneumoniae. Pathogens 8 (4), 1–16

    Not in our library10.3390/pathogens8040277

31. 31.

    Diago-Navarro E. Motley M. P. Ruiz-Perez G. Yu W. Austin J. Seco B. M. S.. (2018 ). Novel, Broadly Reactive Anticapsular Antibodies Against Carbapenem-Resistant Klebsiella Pneumoniae Protect From Infection. mBio 9 (2), 1–11

    Not in our library10.1128/mbio.00091-18

32. 32.

    Di Martino P. Cafferini N. Joly B. Darfeuille-Michaud A. (2003 ). Klebsiella Pneumoniae Type 3 Pili Facilitate Adherence and Biofilm Formation on Abiotic Surfaces. Res. Microbiol. 154 (1), 9–16

    Not in our library10.1016/s0923-2508(02)00004-9

33. 33.

    Donlan R. M. (2001 ). Biofilm Formation: A Clinically Relevant Microbiological Process. Clin. Infect. Dis. 33 (8), 1387–1392

    Not in our library10.1086/322972

34. 34.

    Elias S. Banin E. (2012 ). Multi-Species Biofilms: Living With Friendly Neighbors. FEMS Microbiol. Rev. 36 (5), 990–1004

    Not in our library10.1111/j.1574-6976.2012.00325.x

35. 35.

    Escolar L. Perez-Martin J. de Lorenzo V. (1999 ). Opening the Iron Box: Transcriptional Metalloregulation by the Fur Protein. J. Bacteriol. 181 (20), 6223–6229

    Not in our library10.1128/jb.181.20.6223-6229.1999

36. 36.

    Fang C. T. Chen Y. C. Chang S. C. Sau W. Y. Luh K. T. (2000 ). Klebsiella Pneumoniae Meningitis: Timing of Antimicrobial Therapy and Prognosis. QJM 93 (1), 45–53

    Not in our library10.1093/qjmed/93.1.45

37. 37.

    Flemming H. C. Wingender J. (2010 ). The Biofilm Matrix. Nat. Rev. Microbiol. 8 (9), 623–633

    Not in our library10.1038/nrmicro2415

38. 38.

    Flemming H. C. Wingender J. Szewzyk U. Steinberg P. Rice S. A. Kjelleberg S. (2016 ). Biofilms: An Emergent Form of Bacterial Life. Nat. Rev. Microbiol. 14 (9), 563–575

    Not in our library10.1038/nrmicro.2016.94

39. 39.

    Fux C. A. Costerton J. W. Stewart P. S. Stoodley P. (2005 ). Survival Strategies of Infectious Biofilms. Trends Microbiol. 13 (1), 34–40

    Not in our library10.1016/j.tim.2004.11.010

40. 40.

    Gomes A. E. I. Pacheco T. Dos Santos C. D. S. Pereira J. A. Ribeiro M. L. Darrieux M.. (2020 ). Functional Insights From KpfR, a New Transcriptional Regulator of Fimbrial Expression That Is Crucial for Klebsiella Pneumoniae Pathogenicity. Front. Microbiol. 11, 601921

    Not in our library10.3389/fmicb.2020.601921

41. 41.
    Anti-biofilm activity: a function of Klebsiella pneumoniae capsular polysaccharide. · 2014

    Not checked
42. 42.

    Goodwine J. Gil J. Doiron A. Valdes J. Solis M. Higa A.. (2019 ). Pyruvate-Depleting Conditions Induce Biofilm Dispersion and Enhance the Efficacy of Antibiotics in Killing Biofilms In Vitro and In Vivo. Sci. Rep. 9 (1), 3763

    Not in our library10.1038/s41598-019-40378-z

43. 43.

    Guilhen C. Charbonnel N. Parisot N. Gueguen N. Iltis A. Forestier C.. (2016 ). Transcriptional Profiling of Klebsiella Pneumoniae Defines Signatures for Planktonic, Sessile and Biofilm-Dispersed Cells. BMC Genomics 17, 237

    Not in our library10.1186/s12864-016-2557-x

44. 44.

    Guilhen C. Miquel S. Charbonnel N. Joseph L. Carrier G. Forestier C.. (2019 ). Colonization and Immune Modulation Properties of Klebsiella Pneumoniae Biofilm-Dispersed Cells. NPJ Biofilms. Microbiomes. 5 (1), 25

    Not in our library10.1038/s41522-019-0098-1

45. 45.

    Gurjala A. N. Geringer M. R. Seth A. K. Hong S. J. Smeltzer M. S. Galiano R. D.. (2011 ). Development of a Novel, Highly Quantitative In Vivo Model for the Study of Biofilm-Impaired Cutaneous Wound Healing. Wound Repair Regener. 19 (3), 400–410

    Not in our library10.1111/j.1524-475x.2011.00690.x

46. 46.

    Hall-Stoodley L. Costerton J. W. Stoodley P. (2004 ). Bacterial Biofilms: From the Natural Environment to Infectious Diseases. Nat. Rev. Microbiol. 2 (2), 95–108

    Not in our library10.1038/nrmicro821

47. 47.

    Hancock V. Dahl M. Klemm P. (2010 ). Abolition of Biofilm Formation in Urinary Tract Escherichia Coli and Klebsiella Isolates by Metal Interference Through Competition for Fur. Appl. Environ. Microbiol. 76 (12), 3836–3841

    Not in our library10.1128/aem.00241-10

48. 48.

    Jagnow J. Clegg S. (2003 ). Klebsiella Pneumoniae MrkD-Mediated Biofilm Formation on Extracellular Matrix- and Collagen-Coated Surfaces. Microbiol. (Reading). 149 (Pt 9), 2397–2405

    Not in our library10.1099/mic.0.26434-0

49. 49.

    Jamal M. Ahmad W. Andleeb S. Jalil F. Imran M. Nawaz M. A.. (2018 ). Bacterial Biofilm and Associated Infections. J. Chin. Med. Assoc. 81 (1), 7–11

    Not in our library10.1016/j.jcma.2017.07.012

50. 50.

    Johnson J. G. Murphy C. N. Sippy J. Johnson T. J. Clegg S. (2011 ). Type 3 Fimbriae and Biofilm Formation are Regulated by the Transcriptional Regulators MrkHI in Klebsiella Pneumoniae. J. Bacteriol. 193 (14), 3453–3460

    Not in our library10.1128/jb.00286-11

51. 51.

    Joshi R. V. Gunawan C. Mann R. (2021 ). We Are One: Multispecies Metabolism of a Biofilm Consortium and Their Treatment Strategies. Front. Microbiol. 12, 635432

    Not in our library10.3389/fmicb.2021.635432

52. 52.

    Kania R. E. Lamers G. E. Dijkhuizen N. M. Lagendijk E. Huy P. T.. (2010 ). Biofilms on Tracheoesophageal Voice Prostheses: A Confocal Laser Scanning Microscopy Demonstration of Mixed Bacterial and Yeast Biofilms. Biofouling 26 (5), 519–526

    Not in our library10.1080/08927014.2010.489238

53. 53.

    Karygianni L. Ren Z. Koo H. Thurnheer T. (2020 ). Biofilm Matrixome: Extracellular Components in Structured Microbial Communities. Trends Microbiol. 28 (8), 668–681

    Not in our library10.1016/j.tim.2020.03.016

54. 54.
    In silico analysis of usher encoding genes in Klebsiella pneumoniae and characterization of their role in adhesion and colonization. · 2015

    Not checked
55. 55.

    Klemm P. Schembri M. A. (2000 ). Bacterial Adhesins: Function and Structure. Int. J. Med. Microbiol. 290 (1), 27–35

    Not in our library10.1016/s1438-4221(00)80102-2

56. 56.
    Commensal Protection of Staphylococcus aureus against Antimicrobials by Candida albicans Biofilm Matrix · 2016

    No notice
57. 57.

    Koo H. Yamada K. M. (2016 ). Dynamic Cell-Matrix Interactions Modulate Microbial Biofilm and Tissue 3D Microenvironments. Curr. Opin. Cell Biol. 42, 102–112

    Not in our library10.1016/j.ceb.2016.05.005

58. 58.
    The virulence of Streptococcus mutans and the ability to form biofilms · 2013

    No notice
59. 59.

    Lalitha C. Raman T. Rathore S. S. Ramar M. Munusamy A. Ramakrishnan J. (2017 ). ASK2 Bioactive Compound Inhibits MDR Klebsiella Pneumoniae by Antibiofilm Activity, Modulating Macrophage Cytokines and Opsonophagocytosis. Front. Cell Infect. Microbiol. 7, 346

    Not in our library10.3389/fcimb.2017.00346

60. 60.

    Lee K. W. Periasamy S. Mukherjee M. Xie C. Kjelleberg S. Rice S. A. (2014 ). Biofilm Development and Enhanced Stress Resistance of a Model, Mixed-Species Community Biofilm. ISME. J. 8 (4), 894–907

    Not in our library10.1038/ismej.2013.194

61. 61.

    Lin T. H. Tseng C. Y. Lai Y. C. Wu C. C. Huang C. F. Lin C. T. (2017 ). IscR Regulation of Type 3 Fimbriae Expression in Klebsiella Pneumoniae CG43. Front. Microbiol. 8, 1984

    Not in our library10.3389/fmicb.2017.01984

62. 62.

    Lohse M. B. Gulati M. Johnson A. D. Nobile C. J. (2018 ). Development and Regulation of Single- and Multi-Species Candida Albicans Biofilms. Nat. Rev. Microbiol. 16 (1), 19–31

    Not in our library10.1038/nrmicro.2017.107

63. 63.

    Luo T. L. Vanek M. E. Gonzalez-Cabezas C. Marrs C. F. Foxman B. Rickard A. H. (2022 ). In Vitro Model Systems for Exploring Oral Biofilms: From Single-Species Populations to Complex Multi-Species Communities. J. Appl. Microbiol. 132 (2), 855–871

    Not in our library10.1111/jam.15200

64. 64.

    Macleod S. M. Stickler D. J. (2007 ). Species Interactions in Mixed-Community Crystalline Biofilms on Urinary Catheters. J. Med. Microbiol. 56 (Pt 11), 1549–1557

    Not in our library10.1099/jmm.0.47395-0

65. 65.

    Majik M. S. Parvatkar P. T. (2014 ). Next Generation Biofilm Inhibitors for Pseudomonas Aeruginosa: Synthesis and Rational Design Approaches. Curr. Top. Med. Chem. 14 (1), 81–109

    Not in our library10.2174/1568026613666131113152257

66. 66.

    Marks L. R. Mashburn-Warren L. Federle M. J. Hakansson A. P. (2014 ). Streptococcus Pyogenes Biofilm Growth In Vitro and In Vivo and its Role in Colonization, Virulence, and Genetic Exchange. J. Infect. Dis. 210 (1), 25–34

    Not in our library10.1093/infdis/jiu058

67. 67.

    Martin M. L. Dassie S. A. Valenti L. E. Giacomelli C. E. (2019 ). A Simple Surface Biofunctionalization Strategy to Inhibit the Biofilm Formation by Staphylococcus Aureus on Solid Substrates. Colloids. Surf. B. Biointerfaces. 183, 110432

    Not in our library10.1016/j.colsurfb.2019.110432

68. 68.

    Miller M. B. Bassler B. L. (2001 ). Quorum Sensing in Bacteria. Annu. Rev. Microbiol. 55, 165–199

    Not in our library10.1146/annurev.micro.55.1.165

69. 69.

    Mirzaei R. Ranjbar R. (2022 ). Hijacking Host Components for Bacterial Biofilm Formation: An Advanced Mechanism. Int. Immunopharmacol. 103, 108471

    Not in our library10.1016/j.intimp.2021.108471

70. 70.

    Monds R. D. O'Toole G. A. (2009 ). The Developmental Model of Microbial Biofilms: Ten Years of a Paradigm Up for Review. Trends Microbiol. 17 (2), 73–87

    Not in our library10.1016/j.tim.2008.11.001

71. 71.

    Mukherjee S. Bassler B. L. (2019 ). Bacterial Quorum Sensing in Complex and Dynamically Changing Environments. Nat. Rev. Microbiol. 17 (6), 371–382

    Not in our library10.1038/s41579-019-0186-5

72. 72.

    Murphy C. N. Mortensen M. S. Krogfelt K. A. Clegg S. (2013 ). 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. 81 (8), 3009–3017

    Not in our library10.1128/iai.00348-13

73. 73.

    Nait Chabane Y. Marti S. Rihouey C. Alexandre S. Hardouin J. Lesouhaitier O.. (2014 ). Characterisation of Pellicles Formed by Acinetobacter Baumannii at the Air-Liquid Interface. PloS One 9 (10), e111660

    Not in our library10.1371/journal.pone.0111660

74. 74.
    Biofilm formation and antibiotic resistance of Klebsiella pneumoniae isolated from clinical samples in a tertiary care hospital, Klaten, Indonesia · 2019

    No notice
75. 75.

    Okshevsky M. Regina V. R. Meyer R. L. (2015 ). Extracellular DNA as a Target for Biofilm Control. Curr. Opin. Biotechnol. 33, 73–80

    Not in our library10.1016/j.copbio.2014.12.002

76. 76.

    Ostria-Hernandez M. L. Juarez-de la Rosa K. C. Arzate-Barbosa P. Lara-Hernandez A. Sakai F. Ibarra J. A.. (2018 ). Nosocomial, Multidrug-Resistant Klebsiella Pneumoniae Strains Isolated From Mexico City Produce Robust Biofilms on Abiotic Surfaces But Not on Human Lung Cells. Microb. Drug Resist. 24 (4), 422–433

    Not in our library10.1089/mdr.2017.0073

77. 77.
    SdiA, a Quorum-Sensing Regulator, Suppresses Fimbriae Expression, Biofilm Formation, and Quorum-Sensing Signaling Molecules Production in Klebsiella pneumoniae · 2021

    Not checked
78. 78.

    Paczosa M. K. Mecsas J. (2016 ). Klebsiella Pneumoniae: Going on the Offense With a Strong Defense. Microbiol. Mol. Biol. Rev. 80 (3), 629–661

    Not in our library10.1128/mmbr.00078-15

79. 79.
    Interactions of Methicillin Resistant Staphylococcus aureus USA300 and Pseudomonas aeruginosa in Polymicrobial Wound Infection · 2013

    No notice
80. 80.

    Periasamy S. Nair H. A. Lee K. W. Ong J. Goh J. Q. Kjelleberg S.. (2015 ). Pseudomonas Aeruginosa PAO1 Exopolysaccharides are Important for Mixed Species Biofilm Community Development and Stress Tolerance. Front. Microbiol. 6, 851

    Not in our library10.3389/fmicb.2015.00851

81. 81.

    Piperaki E. T. Syrogiannopoulos G. A. Tzouvelekis L. S. Daikos G. L. (2017 ). Klebsiella Pneumoniae: Virulence, Biofilm and Antimicrobial Resistance. Pediatr. Infect. Dis. J. 36 (10), 1002–1005

    Not in our library10.1097/inf.0000000000001675

82. 82.

    Ponde N. O. Lortal L. Ramage G. Naglik J. R. Richardson J. P. (2021 ). Candida Albicans Biofilms and Polymicrobial Interactions. Crit. Rev. Microbiol. 47 (1), 91–111

    Not in our library10.1080/1040841x.2020.1843400

83. 83.
    Microbial Species Isolated from Infected Wounds and Antimicrobial Resistance Analysis: Data Emerging from a Three-Years Retrospective Study · 2021

    No notice
84. 84.

    Rabin N. Zheng Y. Opoku-Temeng C. Du Y. Bonsu E. Sintim H. O. (2015 ). Biofilm Formation Mechanisms and Targets for Developing Antibiofilm Agents. Future Med. Chem. 7 (4), 493–512

    Not in our library10.4155/fmc.15.6

85. 85.

    Roberts A. P. Kreth J. (2014 ). The Impact of Horizontal Gene Transfer on the Adaptive Ability of the Human Oral Microbiome. Front. Cell Infect. Microbiol. 4, 124

    Not in our library10.3389/fcimb.2014.00124

86. 86.

    Roder H. L. Sorensen S. J. Burmolle M. (2016 ). Studying Bacterial Multispecies Biofilms: Where to Start? Trends Microbiol. 24 (6), 503–513

    Not in our library10.1016/j.tim.2016.02.019

87. 87.

    Rosen D. A. Pinkner J. S. Jones J. M. Walker J. N. Clegg S. Hultgren S. J. (2008 ). 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. 76 (7), 3337–3345

    Not in our library10.1128/iai.00090-08

88. 88.

    Russo T. A. MacDonald U. (2020 ). The Galleria Mellonella Infection Model Does Not Accurately Differentiate Between Hypervirulent and Classical Klebsiella Pneumoniae. mSphere 5 (1), 1–7

    Not in our library10.1128/msphere.00850-19

89. 89.

    Russo T. A. Marr C. M. (2019 ). Hypervirulent Klebsiella Pneumoniae. Clin. Microbiol. Rev. 32 (3), 1–42

    Not in our library10.1128/cmr.00001-19

90. 90.

    Russo T. A. Olson R. Macdonald U. Metzger D. Maltese L. M. Drake E. J.. (2014 ). Aerobactin Mediates Virulence and Accounts for Increased Siderophore Production Under Iron-Limiting Conditions by Hypervirulent (Hypermucoviscous) Klebsiella Pneumoniae. Infect. Immun. 82 (6), 2356–2367

    Not in our library10.1128/iai.01667-13

91. 91.

    Santiago A. J. Burgos-Garay M. L. Kartforosh L. Mazher M. Donlan R. M. (2020 ). Bacteriophage Treatment of Carbapenemase-Producing Klebsiella Pneumoniae in a Multispecies Biofilm: A Potential Biocontrol Strategy for Healthcare Facilities. AIMS. Microbiol. 6 (1), 43–63

    Not in our library10.3934/microbiol.2020003

92. 92.

    Saxena P. Joshi Y. Rawat K. Bisht R. (2019 ). Biofilms: Architecture, Resistance, Quorum Sensing and Control Mechanisms. Indian J. Microbiol. 59 (1), 3–12

    Not in our library10.1007/s12088-018-0757-6

93. 93.

    Schembri M. A Blom J. Krogfelt K. A Klemm P. (2005 ). Capsule and fimbria interaction in Klebsiella pneumoniae. Infect Immun. 73 (8), 4626–33

    Not in our library10.1007/s12088-018-0757-6

94. 94.

    Schembri M. A Dalsgaard D. Klemm P. (2004 ). Capsule shields the function of short bacterial adhesins. J Bacteriol. 186 (5), 1249–57

    Not in our library10.1128/jb.186.5.1249-1257.2004

95. 95.
    Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation · 2010

    No notice
96. 96.

    Singh A. K. Yadav S. Chauhan B. S. Nandy N. Singh R. Neogi K.. (2019 ). Classification of Clinical Isolates of Klebsiella Pneumoniae Based on Their In Vitro Biofilm Forming Capabilities and Elucidation of the Biofilm Matrix Chemistry With Special Reference to the Protein Content. Front. Microbiol. 10, 669

    Not in our library10.3389/fmicb.2019.00669

97. 97.
    Biofilm formation of Klebsiella pneumoniae on urethral catheters requires either type 1 or type 3 fimbriae · 2012

    No notice
98. 98.

    Stewart P. S. Camper A. K. Handran S. D. Huang C. Warnecke M. (1997 ). Spatial Distribution and Coexistence of Klebsiella Pneumoniae and Pseudomonas Aeruginosa in Biofilms. Microb. Ecol. 33 (1), 2–10

    Not in our library10.1007/s002489900002

99. 99.

    Stickler D. J. Morris N. S. Winters C. (1999 ). [35] Simple Physical Model to Study Formation and Physiology of Biofilms on Urethral Catheters. Biofilms, 310, 494–501

    Not in our library10.1016/s0076-6879(99)10037-5

100. 100.

     Struve C. Bojer M. Krogfelt K. A. (2008 ). Characterization of Klebsiella Pneumoniae Type 1 Fimbriae by Detection of Phase Variation During Colonization and Infection and Impact on Virulence. Infect. Immun. 76 (9), 4055–4065

     Not in our library10.1128/iai.00494-08

101. 101.
     N-Acyl Homoserine Lactone-Mediated Quorum Sensing Regulates Species Interactions in Multispecies Biofilm Communities · 2021

     Not checked
102. 102.

     Thompson J. A. Oliveira R. A. Djukovic A. Ubeda C. Xavier K. B. (2015 ). Manipulation of the Quorum Sensing Signal AI-2 Affects the Antibiotic-Treated Gut Microbiota. Cell Rep. 10 (11), 1861–1871

     Not in our library10.1016/j.celrep.2015.02.049

103. 103.

     Thompson M. G. Truong-Le V. Alamneh Y. A. Black C. C. Anderl J. Honnold C. L.. (2015 ). Evaluation of Gallium Citrate Formulations Against a Multidrug-Resistant Strain of Klebsiella Pneumoniae in a Murine Wound Model of Infection. Antimicrob. Agents Chemother. 59 (10), 6484–6493

     Not in our library10.1128/aac.00882-15

104. 104.

     Touzel R. E. Sutton J. M. Wand M. E. (2016 ). Establishment of a Multi-Species Biofilm Model to Evaluate Chlorhexidine Efficacy. J. Hosp. Infect. 92 (2), 154–160

     Not in our library10.1016/j.jhin.2015.09.013

105. 105.

     Townsend E. M. Moat J. Jameson E. (2020 ). CAUTI's Next Top Model - Model Dependent Klebsiella Biofilm Inhibition by Bacteriophages and Antimicrobials. Biofilm 2, 100038

     Not in our library10.1016/j.bioflm.2020.100038

106. 106.
     Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria · 2013

     No notice
107. 107.

     Vuotto C. Longo F. Pascolini C. Donelli G. Balice M. P. Libori M. F.. (2017 ). Biofilm Formation and Antibiotic Resistance in Klebsiella Pneumoniae Urinary Strains. J. Appl. Microbiol. 123 (4), 1003–1018

     Not in our library10.1111/jam.13533

108. 108.

     Wang Q. Chang C. S. Pennini M. Pelletier M. Rajan S. Zha J.. (2016 ). Target-Agnostic Identification of Functional Monoclonal Antibodies Against Klebsiella Pneumoniae Multimeric MrkA Fimbrial Subunit. J. Infect. Dis. 213 (11), 1800–1808

     Not in our library10.1093/infdis/jiw021

109. 109.

     Wang J. Liu X. Yu K. Liu M. Qu J. Liu Y.. (2022 ). Psl-Dependent Cooperation Contributes to Drug Resistance of Pseudomonas Aeruginosa in Dual-Species Biofilms With Acinetobacter Baumannii. ACS Infect. Dis. 8 (1), 129–136

     Not in our library10.1021/acsinfecdis.1c00416

110. 110.
     The Characteristic of Virulence, Biofilm and Antibiotic Resistance of Klebsiella pneumoniae · 2020

     No notice
111. 111.

     Warrier A. Satyamoorthy K. Murali T. S. (2021 ). Quorum-Sensing Regulation of Virulence Factors in Bacterial Biofilm. Future Microbiol. 16, 1003–1021

     Not in our library10.2217/fmb-2020-0301

112. 112.
     MrkH, a Novel c-di-GMP-Dependent Transcriptional Activator, Controls Klebsiella pneumoniae Biofilm Formation by Regulating Type 3 Fimbriae Expression · 2011

     No notice
113. 113.

     Willsey G. G. Ventrone S. Schutz K. C. Wallace A. M. Ribis J. W. Suratt B. T.. (2018 ). Pulmonary Surfactant Promotes Virulence Gene Expression and Biofilm Formation in Klebsiella Pneumoniae. Infect. Immun. 86 (7), 1–18

     Not in our library10.1128/iai.00135-18

114. 114.

     Wu C. C. Huang Y. J. Fung C. P. Peng H. L. (2010 ). Regulation of the Klebsiella Pneumoniae Kpc Fimbriae by the Site-Specific Recombinase KpcI. Microbiol. (Reading). 156 (Pt 7), 1983–1992

     Not in our library10.1099/mic.0.038158-0

115. 115.

     Wu C. C. Lin C. T. Cheng W. Y. Huang C. J. Wang Z. C. Peng H. L. (2012 ). Fur-Dependent MrkHI Regulation of Type 3 Fimbriae in Klebsiella Pneumoniae CG43. Microbiol. (Reading). 158 (Pt 4), 1045–1056

     Not in our library10.1099/mic.0.053801-0

116. 116.
     Isolation of Genes Involved in Biofilm Formation of a Klebsiella pneumoniae Strain Causing Pyogenic Liver Abscess · 2011

     No notice
117. 117.
     Distinct evolutionary dynamics of horizontal gene transfer in drug resistant and virulent clones of Klebsiella pneumoniae · 2019

     No notice
118. 118.
     Identification of Klebsiella capsule synthesis loci from whole genome data · 2016

     No notice
119. 119.

     Yoshida S. Ogawa N. Fujii T. Tsushima S. (2009 ). Enhanced Biofilm Formation and 3-Chlorobenzoate Degrading Activity by the Bacterial Consortium of Burkholderia Sp. NK8 and Pseudomonas Aeruginosa PAO1. J. Appl. Microbiol. 106 (3), 790–800

     Not in our library10.1111/j.1365-2672.2008.04027.x

120. 120.
     Biofilm Formation in Klebsiella pneumoniae Bacteremia Strains Was Found to be Associated with CC23 and the Presence of wcaG · 2018

     Not checked

Cited by papers we hold 3

• Immune dysfunction during S. aureus biofilm-associated implant infections: opportunities for novel therapeutic strategies · 2025
  Not checked
• General Overview of Klebsiella pneumonia: Epidemiology and the Role of Siderophores in Its Pathogenicity · 2024
  No notice
• Horizontal Gene Transfer of Antibiotic Resistance Genes in Biofilms · 2023
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.