Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 60

The DOI matches its Crossref record; 14 of the 14 references it cites were found in a registry or an index.

Biofilm Formation by Pathogenic Bacteria: Applying a Staphylococcus aureus Model to Appraise Potential Targets for Therapeutic Intervention

Sedarat, Zahra, Taylor-Robinson, Andrew W.·2022·Pathogens
DOI 10.3390/pathogens11040388
Open this paper in CoChat — free account

Abstract

Carried in the nasal passages by up to 30% of humans, Staphylococcus aureus is recognized to be a successful opportunistic pathogen. It is a frequent cause of infections of the upper respiratory tract, including sinusitis, and of the skin, typically abscesses, as well as of food poisoning and medical device contamination. The antimicrobial resistance of such, often chronic, health conditions is underpinned by the unique structure of bacterial biofilm, which is the focus of increasing research to try to overcome this serious public health challenge. Due to the protective barrier of an exopolysaccharide matrix, bacteria that are embedded within biofilm are highly resistant both to an infected individual’s immune response and to any treating antibiotics. An in-depth appraisal of the stepwise progression of biofilm formation by S. aureus, used as a model infection for all cases of bacterial antibiotic resistance, has enhanced understanding of this complicated microscopic structure and served to highlight possible intervention targets for both patient cure and community infection control. While antibiotic therapy offers a practical means of treatment and prevention, the most favorable results are achieved in combination with other methods. This review provides an overview of S. aureus biofilm development, outlines the current range of anti-biofilm agents that are used against each stage and summarizes their relative merits.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/pathogens11040388

Cites

14 of 14 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 14 references

Research works printed but not linked: 203

  1. Jamal, 2018, Bacterial biofilm and associated infections, J. Chin. Med. Assoc., 81, 7, 10.1016/j.jcma.2017.07.012 · DOI · Paper page
  2. Slavkin, 1997, Biofilms, microbial ecology and Antoni van Leeuwenhoek, J. Am. Dent. Assoc., 128, 492, 10.14219/jada.archive.1997.0238 · doi:10.14219/jada.archive.1997.0238
  3. Sedarat, 2019, A Consideration of antibacterial agent efficacies in the treatment and prevention of formation of Staphylococcus aureus biofilm, J. Microbiol. Infect. Dis., 9, 167, 10.5799/jmid.657903 · DOI
  4. Hadjifrangiskou, 2012, What does it take to stick around? Molecular insights into biofilm formation by uropathogenic Escherichia coli, Virulence, 3, 231, 10.4161/viru.19763 · DOI
  5. Jefferson, 2004, What drives bacteria to produce a biofilm?, FEMS Microbiol. Lett., 236, 163, 10.1111/j.1574-6968.2004.tb09643.x · DOI · Paper page
  6. Percival, S.L., Randle, J., Cooper, T., and Williams, D.W. (2014). Biofilms: From concept to reality. Biofilms in Infection Prevention and Control, Academic Press.
  7. 2014, Biofilms as a mechanism of bacterial resistance, Drug Discov. Today Technol., 11, 49, 10.1016/j.ddtec.2014.02.003 · DOI · Paper page
  8. Donlan, 2002, Biofilms: Microbial life on surfaces, Emerg. Infect. Dis., 8, 881, 10.3201/eid0809.020063 · DOI · Paper page
  9. Tong, 2015, Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management, Clin. Microbiol. Rev., 28, 603, 10.1128/CMR.00134-14 · DOI · Paper page
  10. Zecconi, 2013, Staphylococcus aureus virulence factors in evasion from innate immune defenses in human and animal diseases, Immunol. Lett., 150, 12, 10.1016/j.imlet.2013.01.004 · DOI · Paper page
  11. Lister, 2014, Staphylococcus aureus biofilms: Recent developments in biofilm dispersal, Front. Cell. Infect. Microbiol., 4, 178, 10.3389/fcimb.2014.00178 · DOI · Paper page
  12. Mah, 2001, Mechanisms of biofilm resistance to antimicrobial agents, Trends Microbiol., 9, 34, 10.1016/S0966-842X(00)01913-2 · DOI · Paper page
  13. Manandhar, 2018, Biofilm producing clinical Staphylococcus aureus isolates augmented prevalence of antibiotic resistant cases in tertiary care hospitals of Nepal, Front. Microbiol., 9, 2749, 10.3389/fmicb.2018.02749 · DOI
  14. Ciofu, 2010, Pseudomonas aeruginosa biofilms in cystic fibrosis, Future Microbiol., 5, 1663, 10.2217/fmb.10.125 · DOI · Paper page
  15. Foxman, 2010, The epidemiology of urinary tract infection, Nat. Rev. Urol., 7, 653, 10.1038/nrurol.2010.190 · DOI · Paper page
  16. MacKenzie, 2017, Examining the link between biofilm formation and the ability of pathogenic Salmonella strains to colonize multiple host species, Front. Vet. Sci., 4, 138, 10.3389/fvets.2017.00138 · DOI
  17. Lemon, 2007, Flagellar motility is critical for Listeria monocytogenes biofilm formation, J. Bacteriol., 189, 4418, 10.1128/JB.01967-06 · DOI · Paper page
  18. Vlamakis, 2013, Sticking together: Building a biofilm the Bacillus subtilis way, Nat. Rev. Microbiol., 11, 157, 10.1038/nrmicro2960 · DOI · Paper page
  19. Yonezawa, 2010, Assessment of in vitro biofilm formation by Helicobacter pylori, J. Gastroenterol. Hepatol., 25, S90, 10.1111/j.1440-1746.2009.06213.x · doi:10.1111/j.1440-1746.2009.06213.x
  20. Nicolas, 2011, Streptococcus mutans and oral streptococci in dental plaque, Can. J. Microbiol., 57, 1, 10.1139/W10-095 · DOI
  21. Darouiche, 2004, Treatment of infections associated with surgical implants, N. Engl. J. Med., 350, 1422, 10.1056/NEJMra035415 · DOI · Paper page
  22. Mulcahy, 2014, Pseudomonas aeruginosa biofilms in disease, Microb. Ecol., 68, 1, 10.1007/s00248-013-0297-x · DOI · Paper page
  23. Bridier, A., and Briandet, R. (2022). Microbial biofilms: Structural plasticity and emerging properties. Microorganisms, 10. · doi:10.3390/microorganisms10010138
  24. Qu, 2010, Densely adherent growth mode, rather than extracellular polymer substance matrix build-up ability, contributes to high resistance of Staphylococcus epidermidis biofilms to antibiotics, J. Antimicrob. Chemother., 65, 1405, 10.1093/jac/dkq119 · DOI
  25. Ferriol-González, C., and Domingo-Calap, P. (2020). Phages for biofilm removal. Antibiotics, 9. · DOI · Paper page
  26. Melter, 2010, Small colony variants of Staphylococcus aureus—Review, Folia Microbiol., 55, 548, 10.1007/s12223-010-0089-3 · DOI
  27. Serra, 2014, Stress responses go three dimensional—The spatial order of physiological differentiation in bacterial macrocolony biofilms, Environ. Microbiol., 16, 1455, 10.1111/1462-2920.12483 · DOI · Paper page
  28. Bendinger, 1993, Physicochemical cell surface and adhesive properties of coryneform bacteria related to the presence and chain length of mycolic acids, Appl. Environ. Microbiol., 59, 3973, 10.1128/aem.59.11.3973-3977.1993 · DOI · Paper page
  29. Power, 2003, The genetics of glycosylation in Gram-negative bacteria, FEMS Microbiol. Lett., 218, 211, 10.1111/j.1574-6968.2003.tb11520.x · doi:10.1111/j.1574-6968.2003.tb11520.x
  30. Costerton, 1987, Bacterial biofilms in nature and disease, Annu. Rev. Microbiol., 41, 435, 10.1146/annurev.mi.41.100187.002251 · DOI · Paper page
  31. Costerton, 2004, Bacterial biofilms: From the natural environment to infectious diseases, Nat. Rev. Microbiol., 2, 95, 10.1038/nrmicro821 · DOI · Paper page
  32. Flemming, 2010, The biofilm matrix, Nat. Rev. Microbiol., 8, 623, 10.1038/nrmicro2415 · DOI · Paper page
  33. Otto, 2006, Bacterial evasion of antimicrobial peptides by biofilm formation, Curr. Top. Microbiol. Immunol., 306, 251
  34. McConoughey, 2014, Biofilms in periprosthetic orthopedic infections, Future Microbiol., 9, 987, 10.2217/fmb.14.64 · DOI · Paper page
  35. Taylor, 2014, Antibiotic resistance in Pseudomonas aeruginosa biofilms: Towards the development of novel anti-biofilm therapies, J. Biotechnol., 191, 121, 10.1016/j.jbiotec.2014.09.003 · DOI · Paper page
  36. Otto, M. (2018). Staphylococcal biofilms. Microbiol. Spectr., 6. · DOI · Paper page
  37. Gupta, 2016, Biofilm, pathogenesis and prevention—A journey to break the wall: A review, Arch. Microbiol., 198, 1, 10.1007/s00203-015-1148-6 · DOI · Paper page
  38. Navarre, 1994, Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria, Mol. Microbiol., 14, 115, 10.1111/j.1365-2958.1994.tb01271.x · DOI · Paper page
  39. Pozzi, 2007, Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections, J. Clin. Microbiol., 45, 1379, 10.1128/JCM.02280-06 · DOI · Paper page
  40. McDevitt, 1994, Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus, Mol. Microbiol., 11, 237, 10.1111/j.1365-2958.1994.tb00304.x · DOI · Paper page
  41. Zong, 2005, A ‘Collagen Hug’ model for Staphylococcus aureus CNA binding to collagen, EMBO J., 24, 4224, 10.1038/sj.emboj.7600888 · DOI · Paper page
  42. Nguyen, 2000, Staphylococcus aureus protein A recognizes platelet gC1qR/p33: A novel mechanism for staphylococcal interactions with platelets, Infect. Immun., 68, 2061, 10.1128/IAI.68.4.2061-2068.2000 · DOI · Paper page
  43. Cucarella, 2001, Bap, a Staphylococcus aureus surface protein involved in biofilm formation, J. Bacteriol., 183, 2888, 10.1128/JB.183.9.2888-2896.2001 · DOI · Paper page
  44. Corrigan, 2007, The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation, Microbiology, 153, 2435, 10.1099/mic.0.2007/006676-0 · DOI · Paper page
  45. Kennedy, 2004, Contribution of culture media and chemical properties of polystyrene tissue culture plates to biofilm development by Staphylococcus aureus, J. Med. Microbiol., 53, 1171, 10.1099/jmm.0.45764-0 · DOI
  46. Gross, 2001, Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces, Infect. Immun., 69, 3423, 10.1128/IAI.69.5.3423-3426.2001 · DOI · Paper page
  47. Biswas, 2006, Activity of the major staphylococcal autolysin Atl, FEMS Microbiol. Lett., 259, 260, 10.1111/j.1574-6968.2006.00281.x · DOI · Paper page
  48. Speziale, 2014, Protein-based biofilm matrices in staphylococci, Front. Cell. Infect. Microbiol., 4, 171, 10.3389/fcimb.2014.00171 · DOI · Paper page
  49. Foster, 2014, Adhesion, invasion and evasion: The many functions of the surface proteins of Staphylococcus aureus, Nat. Rev. Microbiol., 12, 49, 10.1038/nrmicro3161 · DOI · Paper page
  50. Busscher, H.J., and van der Mei, H.C. (2012). How do bacteria know they are on a surface and regulate their response to an adhering state?. PLoS Pathog., 8. · DOI · Paper page
  51. Schlievert, 2014, Models matter: The search for an effective Staphylococcus aureus vaccine, Nat. Rev. Microbiol., 12, 585, 10.1038/nrmicro3308 · DOI · Paper page
  52. Moormeier, 2017, Staphylococcus aureus biofilm: A complex developmental organism, Mol. Microbiol., 104, 365, 10.1111/mmi.13634 · DOI · Paper page
  53. Mann, E.E., Rice, K.C., Boles, B.R., Endres, J.L., Ranjit, D., Chandramohan, L., Tsang, L.H., Smeltzer, M.S., Horswill, A.R., and Bayles, K.W. (2009). Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation. PLoS ONE, 4. · DOI · Paper page
  54. Kiedrowski, M.R., Kavanaugh, J.S., Malone, C.L., Mootz, J.M., Voyich, J.M., Smeltzer, M.S., Bayles, K.W., and Horswill, A.R. (2011). Nuclease modulates biofilm formation in community-associated methicillin-resistant Staphylococcus aureus. PLoS ONE, 6. · DOI · Paper page
  55. Ma, L., Conover, M., Lu, H., Parsek, M.R., Bayles, K., and Wozniak, D.J. (2009). Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog., 5. · DOI · Paper page
  56. Rohde, 2007, Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections, Biomaterials, 28, 1711, 10.1016/j.biomaterials.2006.11.046 · DOI · Paper page
  57. Pozzi, C., Waters, E.M., Rudkin, J.K., Schaeffer, C.R., Lohan, A.J., Tong, P., Loftus, B.J., Pier, G.B., Fey, P.D., and Massey, R.C. (2012). Methicillin resistance alters the biofilm phenotype and attenuates virulence in Staphylococcus aureus device-associated infections. PLoS Pathog., 8. · DOI · Paper page
  58. Wireman, 1977, Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus, J. Bacteriol., 129, 798, 10.1128/jb.129.2.798-802.1977 · DOI · Paper page
  59. Sugimoto, 2018, Broad impact of extracellular DNA on biofilm formation by clinically isolated methicillin-resistant and -sensitive strains of Staphylococcus aureus, Sci. Rep., 8, 2254, 10.1038/s41598-018-20485-z · DOI · Paper page
  60. Mack, 1996, The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: Purification and structural analysis, J. Bacteriol., 178, 175, 10.1128/jb.178.1.175-183.1996 · DOI · Paper page
  61. Vuong, 2004, A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence, J. Biol. Chem., 279, 54881, 10.1074/jbc.M411374200 · DOI · Paper page
  62. Fitzpatrick, 2005, Evidence for icaADBC-independent biofilm development mechanism in methicillin-resistant Staphylococcus aureus clinical isolates, J. Clin. Microbiol., 43, 1973, 10.1128/JCM.43.4.1973-1976.2005 · DOI · Paper page
  63. Brooks, J.L., and Jefferson, K.K. (2014). Phase variation of poly-N-acetylglucosamine expression in Staphylococcus aureus. PLoS Pathog., 10. · DOI · Paper page
  64. Kaplan, 2000, Biofilm formation as microbial development, Annu. Rev. Microbiol., 54, 49, 10.1146/annurev.micro.54.1.49 · DOI · Paper page
  65. Periasamy, 2012, How Staphylococcus aureus biofilms develop their characteristic structure, Proc. Natl. Acad. Sci. USA, 109, 1281, 10.1073/pnas.1115006109 · DOI · Paper page
  66. Moormeier, 2013, Use of microfluidic technology to analyze gene expression during Staphylococcus aureus biofilm formation reveals distinct physiological niches, Appl. Environ. Microbiol., 79, 3413, 10.1128/AEM.00395-13 · DOI
  67. Vieira, 2010, A review of current and emergent biofilm control strategies, LWT Food Sci. Technol., 43, 573, 10.1016/j.lwt.2009.12.008 · DOI · Paper page
  68. Stewart, 2008, Physiological heterogeneity in biofilms, Nat. Rev. Microbiol., 6, 199, 10.1038/nrmicro1838 · DOI · Paper page
  69. Flemming, 2007, The EPS matrix: The “house of biofilm cells”, J. Bacteriol., 189, 7945, 10.1128/JB.00858-07 · DOI · Paper page
  70. Liaqat, 2019, Biofilm formation, maturation and prevention: A review, J. Bacteriol. Mycol., 6, 1092, 10.26420/jbacteriolmycol.2019.1092 · doi:10.26420/jbacteriolmycol.2019.1092
  71. Mulcahy, H., Charron-Mazenod, L., and Lewenza, S. (2008). Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog., 4. · DOI · Paper page
  72. Christensen, 2009, Inactivation of the rhlA gene in Pseudomonas aeruginosa prevents rhamnolipid production, disabling the protection against polymorphonuclear leukocytes, APMIS, 117, 537, 10.1111/j.1600-0463.2009.02466.x · DOI · Paper page
  73. Harro, 2010, Vaccine development in Staphylococcus aureus: Taking the biofilm phenotype into consideration, FEMS Immunol. Med. Microbiol., 59, 306, 10.1111/j.1574-695X.2010.00708.x · DOI
  74. Raafat, 2019, Fighting Staphylococcus aureus biofilms with monoclonal antibodies, Trends Microbiol., 27, 303, 10.1016/j.tim.2018.12.009 · DOI
  75. Hong, 2021, Smart nanomaterials for treatment of biofilm in orthopedic implants, Front. Bioeng. Biotechnol., 9, 694635, 10.3389/fbioe.2021.694635 · DOI
  76. Kathju, 2014, Bacterial biofilms on implanted suture material are a cause of surgical site infection, Surg. Infect., 15, 592, 10.1089/sur.2013.016 · DOI
  77. Post, 2017, Vancomycin displays time-dependent eradication of mature Staphylococcus aureus biofilms, J. Orthop. Res., 35, 381, 10.1002/jor.23291 · doi:10.1002/jor.23291
  78. Ibberson, 2016, Hyaluronan modulation impacts Staphylococcus aureus biofilm infection, Infect. Immun., 84, 1917, 10.1128/IAI.01418-15 · DOI
  79. Urish, 2014, Pulse lavage is inadequate at removal of biofilm from the surface of total knee arthroplasty materials, J. Arthroplast., 29, 1128, 10.1016/j.arth.2013.12.012 · DOI
  80. Donelli, 2007, Synergistic activity of dispersin B and cefamandole nafate in inhibition of staphylococcal biofilm growth on polyurethanes, Antimicrob. Agents Chemother., 51, 2733, 10.1128/AAC.01249-06 · DOI · Paper page
  81. Gilbert, 1993, Formation and dispersal of bacterial biofilms in vivo and in situ, J. Appl. Bacteriol., 74, 67S, 10.1111/j.1365-2672.1993.tb04343.x · DOI
  82. Otto, 2009, Staphylococcus Epidermidis—The ‘Accidental’ Pathogen, Nat. Rev. Microbiol., 7, 555, 10.1038/nrmicro2182 · DOI · Paper page
  83. Whitchurch, 2002, Extracellular DNA required for bacterial biofilm formation, Science, 295, 1487, 10.1126/science.295.5559.1487 · DOI · Paper page
  84. Tang, 2008, Two thermostable nucleases coexisted in Staphylococcus aureus: Evidence from mutagenesis and in vitro expression, FEMS Microbiol. Lett., 284, 176, 10.1111/j.1574-6968.2008.01194.x · doi:10.1111/j.1574-6968.2008.01194.x
  85. Boles, B.R., and Horswill, A.R. (2008). Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog., 4. · DOI · Paper page
  86. Yarwood, 2004, Quorum sensing in Staphylococcus aureus biofilms, J. Bacteriol., 186, 1838, 10.1128/JB.186.6.1838-1850.2004 · DOI · Paper page
  87. Thoendel, 2011, Peptide signaling in the staphylococci, Chem. Rev., 111, 117, 10.1021/cr100370n · DOI · Paper page
  88. Peschel, 2013, Phenol-soluble modulins and staphylococcal infection, Nat. Rev. Microbiol., 11, 667, 10.1038/nrmicro3110 · DOI · Paper page
  89. Xie, 2000, Intergeneric communication in dental plaque biofilms, J. Bacteriol., 182, 7067, 10.1128/JB.182.24.7067-7069.2000 · DOI
  90. Vuong, 2000, Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus, J. Infect. Dis., 182, 1688, 10.1086/317606 · DOI · Paper page
  91. Kavanaugh, 2016, Impact of environmental cues on staphylococcal quorum sensing and biofilm development, J. Biol. Chem., 291, 12556, 10.1074/jbc.R116.722710 · DOI
  92. Reen, 2018, Coumarin: A novel player in microbial quorum sensing and biofilm formation inhibition, Appl. Microbiol. Biotechnol., 102, 2063, 10.1007/s00253-018-8787-x · DOI · Paper page
  93. Miller, 2001, Quorum sensing in bacteria, Annu. Rev. Microbiol., 55, 165, 10.1146/annurev.micro.55.1.165 · DOI · Paper page
  94. Reading, 2006, Quorum sensing: The many languages of bacteria, FEMS Microbiol. Lett., 254, 1, 10.1111/j.1574-6968.2005.00001.x · DOI · Paper page
  95. Banat, 2014, Microbial biofilms: Biosurfactants as antibiofilm agents, Appl. Microbiol. Biotechnol., 98, 9915, 10.1007/s00253-014-6169-6 · DOI · Paper page
  96. Queck, 2008, RNAIII-independent target gene control by the agr quorum-sensing system: Insight into the evolution of virulence regulation in Staphylococcus aureus, Mol. Cell, 32, 150, 10.1016/j.molcel.2008.08.005 · DOI · Paper page
  97. Suresh, 2019, An update on recent developments in the prevention and treatment of Staphylococcus aureus biofilms, Int. J. Med. Microbiol., 309, 1, 10.1016/j.ijmm.2018.11.002 · DOI · Paper page
  98. Hengzhuang, 2011, Pharmacokinetics/pharmacodynamics of colistin and imipenem on mucoid and nonmucoid Pseudomonas aeruginosa biofilms, Antimicrob. Agents Chemother., 55, 4469, 10.1128/AAC.00126-11 · DOI · Paper page
  99. Ciofu, 2011, The clinical impact of bacterial biofilms, Int. J. Oral Sci., 3, 55, 10.4248/IJOS11026 · DOI · Paper page
  100. Ciofu, 2019, Tolerance and resistance of Pseudomonas aeruginosa biofilms to antimicrobial agents—How P. aeruginosa can escape antibiotics, Front. Microbiol., 10, 913, 10.3389/fmicb.2019.00913 · DOI · Paper page
  101. Høiby, N. (2011). Recent advances in the treatment of Pseudomonas aeruginosa infections in cystic fibrosis. BMC Med., 9. · DOI · Paper page
  102. Sun, 2013, Biofilm-associated infections: Antibiotic resistance and novel therapeutic strategies, Future Microbiol., 8, 877, 10.2217/fmb.13.58 · DOI · Paper page
  103. Ciofu, 2017, Antibiotic treatment of biofilm infections, APMIS, 125, 304, 10.1111/apm.12673 · DOI · Paper page
  104. Ranall, 2012, Resolving biofilm infections: Current therapy and drug discovery strategies, Curr. Drug Targets, 13, 1375, 10.2174/138945012803530251 · DOI
  105. Lebeaux, 2014, Biofilm-related infections: Bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics, Microbiol. Mol. Biol. Rev., 78, 510, 10.1128/MMBR.00013-14 · DOI · Paper page
  106. Stewart, 2001, Antibiotic resistance of bacteria in biofilms, Lancet, 358, 135, 10.1016/S0140-6736(01)05321-1 · DOI · Paper page
  107. Williams, 1997, The effects of adherence to silicone surfaces on antibiotic susceptibility in Staphylococcus aureus, Microbiology, 143, 2407, 10.1099/00221287-143-7-2407 · DOI
  108. Thieme, 2019, MBEC versus MBIC: The lack of differentiation between biofilm reducing and inhibitory effects as a current problem in biofilm methodology, Biol. Proced. Online, 21, 18, 10.1186/s12575-019-0106-0 · DOI
  109. Howlin, 2015, Antibiotic-loaded synthetic calcium sulfate beads for prevention of bacterial colonization and biofilm formation in periprosthetic infections, Antimicrob. Agents Chemother., 59, 111, 10.1128/AAC.03676-14 · DOI · Paper page
  110. Okeke, 2003, Export of antimicrobial drugs by West African travelers, J. Travel Med., 10, 133, 10.2310/7060.2003.31786 · doi:10.2310/7060.2003.31786
  111. Kot, 2020, Antimicrobial resistance patterns in methicillin-resistant Staphylococcus aureus from patients hospitalized during 2015–2017 in hospitals in Poland, Med. Princ. Pract., 29, 61, 10.1159/000501788 · doi:10.1159/000501788
  112. Brady, 2017, Antibiotic susceptibility of planktonic- and biofilm-grown staphylococci isolated from implant-associated infections: Should MBEC and nature of biofilm formation replace MIC?, J. Med. Microbiol., 66, 461, 10.1099/jmm.0.000466 · DOI
  113. Antunes, 2010, Application of a feasible method for determination of biofilm antimicrobial susceptibility in staphylococci, APMIS, 118, 873, 10.1111/j.1600-0463.2010.02681.x · DOI
  114. Coenye, 2018, Should standardized susceptibility testing for microbial biofilms be introduced in clinical practice?, Clin. Microbiol. Infect., 24, 570, 10.1016/j.cmi.2018.01.003 · DOI
  115. Ghasemian, 2016, Comparison of biofilm formation between methicillin-resistant and methicillin-susceptible isolates of Staphylococcus aureus, Iran. Biomed. J., 20, 175
  116. Stapleton, 2002, Methicillin resistance in Staphylococcus aureus: Mechanisms and modulation, Sci. Prog., 85, 57, 10.3184/003685002783238870 · DOI · Paper page
  117. Rezaei, 2013, Prevalence of biofilm formation among methicillin resistance Staphylococcus aureus isolated from nasal carriers, Jundishapur J. Microbiol., 6, e9601, 10.5812/jjm.9601 · doi:10.5812/jjm.9601
  118. Watanakunakorn, 1984, Mode of action and in-vitro activity of vancomycin, J. Antimicrob. Chemother., 14, 7, 10.1093/jac/14.suppl_D.7 · DOI · Paper page
  119. Costerton, 1999, Bacterial biofilms: A common cause of persistent infections, Science, 284, 1318, 10.1126/science.284.5418.1318 · DOI · Paper page
  120. Vergidis, 2011, Treatment with linezolid or vancomycin in combination with rifampin is effective in an animal model of methicillin-resistant Staphylococcus aureus foreign body osteomyelitis, Antimicrob. Agents Chemother., 55, 1182, 10.1128/AAC.00740-10 · DOI
  121. Peixoto, 2020, Methicillin-resistant Staphylococcus epidermidis isolates with reduced vancomycin susceptibility from bloodstream infections in a neonatal intensive care unit, J. Med. Microbiol., 69, 41, 10.1099/jmm.0.001117 · DOI
  122. Antunes, 2011, High vancomycin resistance among biofilms produced by Staphylococcus species isolated from central venous catheters, Mem. Inst. Oswaldo Cruz, 106, 51, 10.1590/S0074-02762011000100008 · DOI
  123. Thomsen, 2010, Biofilms in chronic infections—A matter of opportunity—Monospecies biofilms in multispecies infections, FEMS Immunol. Med. Microbiol., 59, 324, 10.1111/j.1574-695X.2010.00714.x · DOI · Paper page
  124. Hamad, 2015, Antibiotic susceptibility among Staphylococcus epidermidis isolated from prosthetic joint infections, with focus on doxycycline, APMIS, 123, 1055, 10.1111/apm.12465 · doi:10.1111/apm.12465
  125. 2010, Susceptibility of Staphylococcus aureus biofilms to vancomycin, gemtamicin and rifampin, J. Epidemiol. Mikrobiol. Imunol., 59, 80
  126. Saginur, 2006, Multiple combination bactericidal testing of staphylococcal biofilms from implant-associated infections, Antimicrob. Agents Chemother., 50, 55, 10.1128/AAC.50.1.55-61.2006 · DOI · Paper page
  127. Raad, 2007, Comparative activities of daptomycin, linezolid, and tigecycline against catheter-related methicillin-resistant Staphylococcus bacteremic isolates embedded in biofilm, Antimicrob. Agents Chemother., 51, 1656, 10.1128/AAC.00350-06 · DOI · Paper page
  128. Smith, 2009, Comparison of biofilm-associated cell survival following in vitro exposure of meticillin-resistant Staphylococcus aureus biofilms to the antibiotics clindamycin, daptomycin, linezolid, tigecycline and vancomycin, Int. J. Antimicrob. Agents, 33, 374, 10.1016/j.ijantimicag.2008.08.029 · DOI
  129. Cafiso, 2010, Tigecycline inhibition of a mature biofilm in clinical isolates of Staphylococcus aureus: Comparison with other drugs, FEMS Immunol. Med. Microbiol., 59, 466, 10.1111/j.1574-695X.2010.00701.x · doi:10.1111/j.1574-695x.2010.00701.x
  130. Wang, 2016, Nanomaterials for the treatment of bacterial biofilms, ACS Infect. Dis., 2, 3, 10.1021/acsinfecdis.5b00116 · DOI
  131. Gupta, 2016, Nanoparticle-based antimicrobials: Surface functionality is critical, F1000Research, 5, 364, 10.12688/f1000research.7595.1 · DOI · Paper page
  132. Kirui, 2019, Targeted laser therapy synergistically enhances efficacy of antibiotics against multi-drug resistant Staphylococcus aureus and Pseudomonas aeruginosa biofilms, Nanomedicine, 20, 102018, 10.1016/j.nano.2019.102018 · DOI
  133. Saggu, 2019, Enzymatic degradation of biofilm by metalloprotease from Microbacterium sp. SKS10, Front. Bioeng. Biotechnol., 7, 192, 10.3389/fbioe.2019.00192 · doi:10.3389/fbioe.2019.00192
  134. Hrvatin, 2017, Combating antibiotic resistance: New drugs or alternative therapies?, Can. Med. Assoc. J., 189, E1199, 10.1503/cmaj.109-5469 · doi:10.1503/cmaj.109-5469
  135. Khan, 2021, Challenges of antibiotic resistance biofilms and potential combating strategies: A review, 3 Biotech, 11, 169, 10.1007/s13205-021-02707-w · DOI · Paper page
  136. Bjarnsholt, 2015, ESCMID Study Group for Biofilms and Consulting External Expert Werner Zimmerli. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014, Clin. Microbiol. Infect., 21, S1, 10.1016/j.cmi.2014.10.024 · DOI · Paper page
  137. Fowler, 2013, Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: A randomized trial, JAMA, 309, 1368, 10.1001/jama.2013.3010 · DOI · Paper page
  138. Spellberg, 2012, Development of a vaccine against Staphylococcus aureus, Semin. Immunopathol., 34, 335, 10.1007/s00281-011-0293-5 · DOI
  139. Xiong, 2017, A human biofilm-disrupting monoclonal antibody potentiates antibiotic efficacy in rodent models of both Staphylococcus aureus and Acinetobacter baumannii infections, Antimicrob. Agents Chemother., 61, e00904-17, 10.1128/AAC.00904-17 · DOI
  140. Lam, 2014, Antibodies to PhnD inhibit staphylococcal biofilms, Infect. Immun., 82, 3764, 10.1128/IAI.02168-14 · DOI
  141. Otto, 2010, Novel targeted immunotherapy approaches for staphylococcal infection, Expert Opin. Biol. Ther., 10, 1049, 10.1517/14712598.2010.495115 · DOI
  142. Kaplan, 2012, Recombinant human DNase I decreases biofilm and increases antimicrobial susceptibility in staphylococci, J. Antibiot., 65, 73, 10.1038/ja.2011.113 · DOI · Paper page
  143. Chaignon, 2007, Susceptibility of staphylococcal biofilms to enzymatic treatments depends on their chemical composition, Appl. Microbiol. Biotechnol., 75, 125, 10.1007/s00253-006-0790-y · DOI · Paper page
  144. Iannitti, 2010, Therapeutical use of probiotic formulations in clinical practice, Clin. Nutr., 29, 701, 10.1016/j.clnu.2010.05.004 · DOI · Paper page
  145. Speranza, 2018, Use of design of experiments to optimize the production of microbial probiotic biofilms, PeerJ, 6, e4826, 10.7717/peerj.4826 · DOI
  146. Becirovic, 2018, The effects of a probiotic milk drink on bacterial composition in the supra- and subgingival biofilm: A pilot study, Benef. Microbes, 9, 865, 10.3920/BM2018.0009 · DOI
  147. Wallis, J.K., Krömker, V., and Paduch, J.-H. (2019). Biofilm challenge: Lactic acid bacteria isolated from bovine udders versus staphylococci. Foods, 8. · DOI
  148. Aoudia, 2016, Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: Effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties, Food Microbiol., 53, 51, 10.1016/j.fm.2015.04.009 · DOI · Paper page
  149. Carvalho, 2017, Disruption of Staphylococcus aureus biofilms using rhamnolipid biosurfactants, J. Dairy Sci., 100, 7864, 10.3168/jds.2017-13012 · DOI
  150. Martin, 2016, Effect of mono and di-rhamnolipids on biofilms pre-formed by Bacillus subtilis BBK006, Curr. Microbiol., 73, 183, 10.1007/s00284-016-1046-4 · DOI
  151. Yi, 2019, Rhamnolipid nanoparticles for in vivo drug delivery and photodynamic therapy, Nanomedicine, 19, 12, 10.1016/j.nano.2019.03.015 · DOI
  152. Stevenson, 2016, Effect of biosurfactants on Pseudomonas aeruginosa and Staphylococcus aureus biofilms in a BioFlux channel, Appl. Microbiol. Biotechnol., 100, 5773, 10.1007/s00253-016-7310-5 · DOI
  153. Stevenson, 2016, Pseudomonas aeruginosa biofilm disruption using microbial surfactants, J. Appl. Microbiol., 120, 868, 10.1111/jam.13049 · DOI
  154. Warrier, 2021, Photodynamic therapy to control microbial biofilms, Photodiagnosis Photodyn. Ther., 33, 102090, 10.1016/j.pdpdt.2020.102090 · DOI
  155. Bombeccari, 2013, Photodynamic therapy to treat periimplantitis, Implant Dent., 22, 631, 10.1097/01.id.0000433592.18679.91 · doi:10.1097/01.id.0000433592.18679.91
  156. Wainwright, 1998, Photodynamic antimicrobial chemotherapy (PACT), J. Antimicrob. Chemother., 42, 13, 10.1093/jac/42.1.13 · DOI · Paper page
  157. Widodo, 2016, An in vitro study on disinfection of titanium surfaces, Clin. Oral Implants Res., 27, 1227, 10.1111/clr.12733 · doi:10.1111/clr.12733
  158. Biel, 2011, Antimicrobial photodynamic therapy treatment of chronic recurrent sinusitis biofilms, Int. Forum Allergy Rhinol., 1, 329, 10.1002/alr.20089 · DOI
  159. Zoccolillo, 2016, Antimicrobial photodynamic therapy of S. mutans biofilms attached to relevant dental materials, Lasers Surg. Med., 48, 995, 10.1002/lsm.22534 · doi:10.1002/lsm.22534
  160. Li, 2019, Synergistic in vitro effects of indocyanine green and ethylenediamine tetraacetate-mediated antimicrobial photodynamic therapy combined with antibiotics for resistant bacterial biofilms in diabetic foot infection, Photodiagnosis Photodyn. Ther., 25, 300, 10.1016/j.pdpdt.2019.01.010 · DOI
  161. Li, 2017, Effect of stable antimicrobial nano-silver packaging on inhibiting mildew and in storage of rice, Food Chem., 215, 477, 10.1016/j.foodchem.2016.08.013 · DOI
  162. Wang, 2018, Effect of nano packaging on preservation quality of Nanjing 9108 rice variety at high temperature and humidity, Food Chem., 239, 23, 10.1016/j.foodchem.2017.06.082 · DOI
  163. Li, 2020, Novel magnetic nanocomposites combining selenium and iron oxide with excellent anti-biofilm properties, J. Mater. Sci., 55, 1012, 10.1007/s10853-019-04019-0 · doi:10.1007/s10853-019-04019-0
  164. Xie, 2020, Ag nanoparticles cluster with pH-triggered reassembly in targeting antimicrobial applications, Adv. Funct. Mater., 30, 2000511, 10.1002/adfm.202000511 · DOI · Paper page
  165. Rabea, 2003, Chitosan as antimicrobial agent: Applications and mode of action, Biomacromolecules, 4, 1457, 10.1021/bm034130m · DOI · Paper page
  166. Albayaty, 2019, Enzyme responsive copolymer micelles enhance the anti-biofilm efficacy of the antiseptic chlorhexidine, Int. J. Pharm., 566, 329, 10.1016/j.ijpharm.2019.05.069 · DOI
  167. Raju, 2020, One-pot fabrication of multifunctional catechin@ZIF-L nanocomposite: Assessment of antibiofilm, larvicidal and photocatalytic activities, J. Photochem. Photobiol. B Biol., 203, 111774, 10.1016/j.jphotobiol.2019.111774 · doi:10.1016/j.jphotobiol.2019.111774
  168. Xie, 2020, Near-infrared light-activated phototherapy by gold nanoclusters for dispersing biofilms, ACS Appl. Mater. Interfaces, 12, 9041, 10.1021/acsami.9b21777 · DOI
  169. Sun, 2019, Cytotoxicity-related bioeffects induced by nanoparticles: The role of surface chemistry, Front. Bioeng. Biotechnol., 7, 414, 10.3389/fbioe.2019.00414 · DOI
  170. Sohaebuddin, 2010, Nanomaterial cytotoxicity is composition, size, and cell type dependent, Part. Fibre Toxicol., 7, 22, 10.1186/1743-8977-7-22 · DOI · Paper page
  171. Harper, 2014, Bacteriophages and biofilms, Antibiotics, 3, 270, 10.3390/antibiotics3030270 · DOI · Paper page
  172. Bai, 2016, Biocontrol and rapid detection of food-borne pathogens using bacteriophages and endolysins, Front. Microbiol., 7, 474, 10.3389/fmicb.2016.00474 · DOI
  173. Hu, 2010, Diffusion properties of bacteriophages through agarose gel membrane, Biotechnol. Prog., 26, 1213, 10.1002/btpr.447 · DOI
  174. Cha, 2019, Effective removal of staphylococcal biofilms on various food contact surfaces by Staphylococcus aureus phage endolysin LysCSA13, Food Microbiol., 84, 103245, 10.1016/j.fm.2019.103245 · DOI
  175. Fenton, 2011, Characterization of the staphylococcal bacteriophage lysin CHAP(K), J. Appl. Microbiol., 111, 1025, 10.1111/j.1365-2672.2011.05119.x · DOI
  176. Gutiérrez, D., Ruas-Madiedo, P., Martinez, B., Rodríguez, A., and Garcia, P. (2014). Effective removal of staphylococcal biofilms by the endolysin LysH5. PLoS ONE, 9. · DOI · Paper page
  177. Sass, 2007, Lytic activity of recombinant bacteriophage phi11 and phi12 endolysins on whole cells and biofilms of Staphylococcus aureus, Appl. Environ. Microbiol., 73, 347, 10.1128/AEM.01616-06 · DOI · Paper page
  178. Domenech, 2017, Csl2, a novel chimeric bacteriophage lysin to fight infections caused by Streptococcus suis, an emerging zoonotic pathogen, Sci. Rep., 7, 16506, 10.1038/s41598-017-16736-0 · doi:10.1038/s41598-017-16736-0
  179. Briers, 2015, Role of the pre-neck appendage protein (Dpo7) from phage vB_SepiS-phiIPLA7 as an anti-biofilm agent in staphylococcal species, Front. Microbiol., 6, 1315
  180. Guo, 2017, Identification and characterization of Dpo42, a novel depolymerase derived from the Escherichia coli phage vB_EcoM_ECOO78, Front. Microbiol., 8, 1460, 10.3389/fmicb.2017.01460 · DOI
  181. Lu, 2007, Dispersing biofilms with engineered enzymatic bacteriophage, Proc. Natl. Acad. Sci. USA, 104, 11197, 10.1073/pnas.0704624104 · DOI · Paper page
  182. Tinoco, 2016, Effect of a genetically engineered bacteriophage on Enterococcus faecalis biofilms, Arch. Oral Biol., 71, 80, 10.1016/j.archoralbio.2016.07.001 · DOI
  183. Motlagh, 2016, Biofilm control with natural and genetically-modified phages, World J. Microbiol. Biotechnol., 32, 67, 10.1007/s11274-016-2009-4 · DOI
  184. Hochberg, 2016, Evolutionary rationale for phages as complements of antibiotics, Trends Microbiol., 24, 249, 10.1016/j.tim.2015.12.011 · DOI · Paper page
  185. Tkhilaishvili, 2018, Bacteriophage Sb-1 enhances antibiotic activity against biofilm, degrades exopolysaccharide matrix and targets persisters of Staphylococcus aureus, Int. J. Antimicrob. Agents, 52, 842, 10.1016/j.ijantimicag.2018.09.006 · DOI · Paper page
  186. Coulter, 2014, Effect of bacteriophage infection in combination with tobramycin on the emergence of resistance in Escherichia coli and Pseudomonas aeruginosa biofilms, Viruses, 6, 3778, 10.3390/v6103778 · DOI
  187. Yasir, M., Willcox, M.D.P., and Dutta, D. (2018). Action of antimicrobial peptides against bacterial biofilms. Materials, 11. · DOI · Paper page
  188. Bahar, 2013, Antimicrobial peptides, Pharmaceuticals, 6, 1543, 10.3390/ph6121543 · DOI · Paper page
  189. Korolik, 2012, Inhibition of bacterial biofilm formation and swarming motility by a small synthetic cationic peptide, Antimicrob. Agents Chemother., 56, 2696, 10.1128/AAC.00064-12 · DOI · Paper page
  190. Nagant, 2012, Identification of peptides derived from the human antimicrobial peptide LL-37 active against biofilms formed by Pseudomonas aeruginosa using a library of truncated fragments, Antimicrob. Agents Chemother., 56, 5698, 10.1128/AAC.00918-12 · DOI
  191. Haisma, 2014, LL-37-derived peptides eradicate multidrug-resistant Staphylococcus aureus from thermally wounded human skin equivalents, Antimicrob. Agents Chemother., 58, 4411, 10.1128/AAC.02554-14 · DOI
  192. Dean, 2011, Susceptibility of Pseudomonas aeruginosa biofilm to alpha-helical peptides: D-enantiomer of LL-37, Front. Microbiol., 2, 128, 10.3389/fmicb.2011.00128 · DOI · Paper page
  193. Mataraci, 2012, In vitro activities of antibiotics and antimicrobial cationic peptides alone and in combination against methicillin-resistant Staphylococcus aureus biofilms, Antimicrob. Agents Chemother., 56, 6366, 10.1128/AAC.01180-12 · DOI
  194. Bacalum, 2015, Cationic antimicrobial peptides cytotoxicity on mammalian cells: An analysis using therapeutic index integrative concept, Int. J. Pept. Res. Ther., 21, 47, 10.1007/s10989-014-9430-z · DOI
  195. Cardoso, 2016, Synthetic antibiofilm peptides, Biochim. Biophys. Acta, 1858, 1061, 10.1016/j.bbamem.2015.12.015 · DOI · Paper page
  196. Kong, 2018, Suppression of Staphylococcus aureus biofilm formation and virulence by a benzimidazole derivative, UM-C162, Sci. Rep., 8, 2758, 10.1038/s41598-018-21141-2 · DOI
  197. Yamasaki, R., Kawano, A., Yoshioka, Y., and Ariyoshi, W. (2020). Rhamnolipids and surfactin inhibit the growth or formation of oral bacterial biofilm. BMC Microbiol., 20. · doi:10.1186/s12866-020-02034-9
  198. Monte, 2014, Antimicrobial activity of selected phytochemicals against Escherichia coli and Staphylococcus aureus and their Biofilms, Pathogens, 3, 473, 10.3390/pathogens3020473 · DOI · Paper page
  199. Borges, A., Abreu, A.C., Dias, C., Saavedra, M.J., Borges, F., and Simões, M. (2016). New perspectives on the use of phytochemicals as an emergent strategy to control bacterial infections including biofilms. Molecules, 21. · DOI · Paper page
  200. Wu, 2011, Sulfhydryl compounds reduce Staphylococcus aureus biofilm formation by inhibiting PIA biosynthesis, FEMS Microbiol. Lett., 316, 44, 10.1111/j.1574-6968.2010.02190.x · DOI

200 of 203 shown

Cited by

See all 60

Metadata

Authors
Sedarat, Z., & Taylor-Robinson, A. W.
Venue
Pathogens
Publisher
MDPI AG
Published
2022-03-23
Volume
11
Issue
4
Pages
388
ISSN
2076-0817
DOI
10.3390/pathogens11040388
Cited by
60
References
14
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Biofilm Formation by Pathogenic Bacteria: Applying a Staphylococcus aureus Model to Appraise Potential Targets for Therapeutic Intervention. https://app.cochat.ai/papers/10.3390/pathogens11040388
The paper
Sedarat, Z., & Taylor-Robinson, A. W. (2022). Biofilm Formation by Pathogenic Bacteria: Applying a Staphylococcus aureus Model to Appraise Potential Targets for Therapeutic Intervention. Pathogens. https://doi.org/10.3390/pathogens11040388

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.