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Strategies for combating antibiotic resistance in bacterial biofilms

Grooters, Kayla E., Ku, Jennifer C., Richter, David M., Krinock, Matthew J., Minor, Ashley, Li, Patrick, Kim, Audrey, Sawyer, Robert, Li, Yong·2024·Frontiers in Cellular and Infection Microbiology

Abstract

Biofilms, which are complexes of microorganisms that adhere to surfaces and secrete protective extracellular matrices, wield substantial influence across diverse domains such as medicine, industry, and environmental science. Despite ongoing challenges posed by biofilms in clinical medicine, research in this field remains dynamic and indeterminate. This article provides a contemporary assessment of biofilms and their treatment, with a focus on recent advances, to chronicle the evolving landscape of biofilm research.

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Figure 1 Mechanism of biofilm formation. Environmental conditions lead planktonic bacteria to utilize adhesion machinery to attach to a surface. Quorum sensing between colony members drives upregulation of extracellular matrix formation and changes in metabolic function, irreversibly cementing biofilm to surface and protecting the colony from environmental hazards (e.g., antiseptics, reactive oxygen species (ROS) and antibiotics. Figure made using Biorender.com.
Figure 1 Mechanism of biofilm formation. Environmental conditions lead planktonic bacteria to utilize adhesion machinery to attach to a surface. Quorum sensing between colony members drives upregulation of extracellular matrix formation and changes in metabolic function, irreversibly cementing biofilm to surface and protecting the colony from environmental hazards (e.g., antiseptics, reactive oxygen species (ROS) and antibiotics. Figure made using Biorender.com.CC BY · PubMed Central

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Research works printed but not linked: 79

  1. Akturk, 2019, Synergistic action of phage and antibiotics: parameters to enhance the killing efficacy against mono and dual-species biofilms, Antibiotics, 8, 10.3390/antibiotics8030103 · DOI
  2. An, 2019, Modulation of antibiotic sensitivity and biofilm formation in Pseudomonas aeruginosa by interspecies signal analogues, Nat. Commun., 10, 2334, 10.1038/s41467-019-10271-4 · DOI
  3. Andersson, 2016, Mechanisms and consequences of bacterial resistance to antimicrobial peptides, Drug Resist. Update, 26, 43, 10.1016/J.DRUP.2016.04.002 · DOI
  4. Antonelli, 2019, Reducing the risk of infection after total joint arthroplasty: preoperative optimization, Arthroplasty, 1, 10.1186/s42836-019-0003-7 · DOI
  5. Argyraki, 2018, UV light assisted antibiotics for eradication of in vitro biofilms, Sci. Rep., 8, 10.1038/S41598-018-34340-8 · DOI
  6. Aristotelous, 2022, Biofilm neutrophils interactions under hypoxia: A mathematical modeling study, Math. Biosci., 352, 10.1016/j.mbs.2022.108893 · DOI
  7. Asma, 2022, An overview of biofilm formation-combating strategies and mechanisms of action of antibiofilm agents, Life (Basel)., 12, 10.3390/life12081110 · DOI
  8. Babin, 2017, Selective proteomic analysis of antibiotic-tolerant cellular subpopulations in pseudomonas aeruginosa biofilms, mBio, 8, 10.1128/mBio.01593-17 · DOI
  9. Barnes, 2018, Carcinogens and DNA damage, Biochem. Soc. Trans., 46, 1213, 10.1042/BST20180519 · DOI
  10. Belfield, 2017, Evaluation of combinations of putative anti-biofilm agents and antibiotics to eradicate biofilms of Staphylococcus aureus and Pseudomonas aeruginosa, J. Antimicrobial. Chemother., 72, 2531, 10.1093/jac/dkx192 · DOI
  11. Bernal-Mercado, 2020, Synergistic mode of action of catechin, vanillic and protocatechuic acids to inhibit the adhesion of uropathogenic Escherichia coli on silicone surfaces, J. Appl. Microbiol., 128, 387, 10.1111/jam.14472 · DOI
  12. Bhattacharya, 2015, Prevention and treatment of Staphylococcus aureus biofilms, Expert Rev. Anti Infect. Ther., 13, 1499, 10.1586/14787210.2015.1100533 · DOI
  13. Cámara, 2022, Economic significance of biofilms: a multidisciplinary and cross-sectoral challenge, NPJ Biofilms. Microbiomes., 8, 42, 10.1038/s41522-022-00306-y · DOI
  14. Castillo-Juárez, 2022, Antimicrobial peptides properties beyond growth inhibition and bacterial killing, PeerJ, 10, 10.7717/PEERJ.12667 · DOI
  15. Cesta, 2020, Bacteriophage therapy: an overview and the position of Italian Society of Infectious and Tropical Diseases, Infez. Med., 28, 322
  16. Charani, 2019, Antibiotic stewardship—Twenty years in the making, Antibiotics, 8, 10.3390/antibiotics8010007 · DOI
  17. Ciofu, 2022, Tolerance and resistance of microbial biofilms, Nat. Rev. Microbiol., 20, 621, 10.1038/s41579-022-00682-4 · DOI
  18. Ciofu, 2017, Antibiotic treatment of biofilm infections, APMIS, 125, 304, 10.1111/apm.12673 · DOI
  19. Clarke, 2020, The safety and efficacy of phage therapy for bone and joint infections: A systematic review, Antibiot. (Basel)., 9, 1, 10.3390/ANTIBIOTICS9110795 · DOI
  20. Conner-Kerr, 1998, The effects of ultraviolet radiation on antibiotic-resistant bacteria in vitro, Ostomy. Wound Manage., 44, 50
  21. Diaconu, 2018, Endotracheal tube biofilm and its impact on the pathogenesis of ventilator-associated pneumonia, J. Crit. Care Med., 4, 50, 10.2478/jccm-2018-0011 · DOI
  22. Di Somma, 2020, Antimicrobial and antibiofilm peptides, Biomolecules, 10, 10.3390/BIOM10040652 · DOI
  23. Doub, 2020, Bacteriophage therapy for clinical biofilm infections: parameters that influence treatment protocols and current treatment approaches, Antibiot. (Basel)., 9, 1, 10.3390/ANTIBIOTICS9110799 · DOI
  24. Ghorbani, 2018, Photosensitizers in antibacterial photodynamic therapy: an overview, Laser. Ther., 27, 293, 10.5978/islsm.27_18-RA-01 · DOI
  25. Ghosh, 2019, Phosphate deficiency induced biofilm formation of Burkholderia on insoluble phosphate granules plays a pivotal role for maximum release of soluble phosphate, Sci. Rep., 9, 5477, 10.1038/s41598-019-41726-9 · DOI
  26. Gimza, 2019, Mapping the global network of extracellular protease regulation in staphylococcus aureus, mSphere, 4, 10.1128/mSphere.00676-19 · DOI
  27. Gominet, 2017, Central venous catheters and biofilms: where do we stand in 2017, APMIS, 125, 365, 10.1111/apm.12665 · DOI
  28. Hall, 2017, Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria, FEMS Microbiol. Rev., 41, 276, 10.1093/femsre/fux010 · DOI
  29. Hou, 2018, Extracellular Polymeric Matrix Production and Relaxation under Fluid Shear and Mechanical Pressure in Staphylococcus aureus Biofilms, Appl. Environ. Microbiol., 84, 10.1128/AEM.01516-17 · DOI
  30. Huigens, 2018, The path to new halogenated quinolines with enhanced activities against staphylococcus epidermidis, Microbiol. Insights, 11, 10.1177/1178636118808532 · DOI
  31. Ielapi, 2020, The role of biofilm in central venous catheter related bloodstream infections: evidence-based nursing and review of the literature, Rev. Recent Clin. Trials., 15, 22, 10.2174/1574887114666191018144739 · DOI
  32. Jacqueline, 2014, Impact of bacterial biofilm on the treatment of prosthetic joint infections, J. Antimicrobial. Chemother., 69, i37, 10.1093/jac/dku254 · DOI
  33. Jamal, 2018, Bacterial biofilm and associated infections, J. Chin. Med. Assoc., 81, 7, 10.1016/j.jcma.2017.07.012 · DOI
  34. Jang, 2016, Endogenous hydrogen peroxide increases biofilm formation by inducing exopolysaccharide production in Acinetobacter oleivorans DR1, Sci. Rep., 6, 10.1038/srep21121 · DOI
  35. Kim, 2016, Essential oils and eugenols inhibit biofilm formation and the virulence of escherichia coli O157:H7, Sci. Rep., 6, 10.1038/srep36377 · DOI
  36. Kirketerp-Møller, 2020, The zone model: A conceptual model for understanding the microenvironment of chronic wound infection, Wound Repair Regener., 28, 593, 10.1111/wrr.12841 · DOI
  37. Kvist, 2008, Inactivation of efflux pumps abolishes bacterial biofilm formation, Appl. Environ. Microbiol., 74, 7376, 10.1128/AEM.01310-08 · DOI
  38. Lamret, 2021, Staphylococcus aureus strain-dependent biofilm formation in bone-like environment, Front. Microbiol., 12, 10.3389/fmicb.2021.714994 · DOI
  39. Lee, 2022, Lipid-coated hybrid nanoparticles for enhanced bacterial biofilm penetration and antibiofilm efficacy, ACS Omega., 7, 35814, 10.1021/acsomega.2c04008 · DOI
  40. Li, 2020, Recombination of T4-like Phages and Its Activity against Pathogenic Escherichia coli in Planktonic and Biofilm Forms, Virol. Sin., 35, 651, 10.1007/s12250-020-00233-2 · DOI
  41. Liu, 2022, Cluster differences in antibiotic resistance, biofilm formation, mobility, and virulence of clinical enterobacter cloacae complex, Front. Microbiol., 13, 10.3389/fmicb.2022.814831 · DOI
  42. Liu, 2015, Metabolic co-dependence gives rise to collective oscillations within biofilms, Nature, 523, 550, 10.1038/nature14660 · DOI
  43. Liu, 2017, Inactivation of a putative efflux pump (LmrB) in Streptococcus mutans results in altered biofilm structure and increased exopolysaccharide synthesis: implications for biofilm resistance, Biofouling, 33, 481, 10.1080/08927014.2017.1323206 · DOI
  44. Luo, 2021, Mechanism of antimicrobial peptides: antimicrobial, anti-inflammatory and antibiofilm activities, Int. J. Mol. Sci., 22, 10.3390/IJMS222111401 · DOI
  45. Malone, 2017, The prevalence of biofilms in chronic wounds: a systematic review and meta-analysis of published data, J. Wound Care, 26, 20, 10.12968/jowc.2017.26.1.20 · DOI
  46. Metcalf, 2013, Biofilm delays wound healing: A review of the evidence, Burns. Trauma, 1, 5, 10.4103/2321-3868.113329 · DOI
  47. Miyaue, 2018, Bacterial memory of persisters: bacterial persister cells can retain their phenotype for days or weeks after withdrawal from colony–biofilm culture, Front. Microbiol., 9, 10.3389/fmicb.2018.01396 · DOI
  48. Namgoong, 2020, Clinical experience with surgical debridement and simultaneous meshed skin grafts in treating biofilm-associated infection: an exploratory retrospective pilot study, J. Plast. Surg. Handb. Surg., 54, 47, 10.1080/2000656X.2019.1673170 · DOI
  49. Nishino, 2021, Function and inhibitory mechanisms of multidrug efflux pumps, Front. Microbiol., 12, 10.3389/fmicb.2021.737288 · DOI
  50. Olsen, 2015, Biofilm-specific antibiotic tolerance and resistance, Eur. J. Clin. Microbiol. Infect. Dis., 34, 877, 10.1007/s10096-015-2323-z · DOI
  51. Ousey, 2023, Comparing methods of debridement for removing biofilm in hard-to-heal wounds, J. Wound Care, 32, S4, 10.12968/jowc.2023.32.Sup3b.S4 · DOI
  52. Overhage, 2008, Human host defense peptide LL-37 prevents bacterial biofilm formation, Infect. Immun., 76, 4176, 10.1128/IAI.00318-08 · DOI
  53. Pallin, 2014, US population aging and demand for inpatient services, J. Hosp. Med., 9, 193, 10.1002/jhm.2145 · DOI
  54. Panlilio, 2021, The role of extracellular DNA in the formation, architecture, stability, and treatment of bacterial biofilms, Biotechnol. Bioeng., 118, 2129, 10.1002/bit.27760 · DOI
  55. Perry, 2023, Bacterial biofilms in the human body: prevalence and impacts on health and disease, Front. Cell Infect. Microbiol., 13, 10.3389/fcimb.2023.1237164 · DOI
  56. Pinto, 2020, Innovative strategies toward the disassembly of the EPS matrix in bacterial biofilms, Front. Microbiol., 11, 10.3389/fmicb.2020.00952 · DOI
  57. Preda, 2019, Communication is the key: biofilms, quorum sensing, formation and prevention, Discoveries. (Craiova)., 7, 10.15190/d.2019.13 · DOI
  58. Rather, 2021, Microbial biofilm: formation, architecture, antibiotic resistance, and control strategies, Braz. J. Microbiol., 52, 1701, 10.1007/s42770-021-00624-x · DOI
  59. Rodríguez-Merchán, 2021, Recent strategies to combat infections from biofilm-forming bacteria on orthopaedic implants, Int. J. Mol. Sci., 22, 10.3390/ijms221910243 · DOI
  60. Saksena, 2019, Follow-up and management of valvular heart disease patients with prosthetic valve: a clinical practice guideline for Indian scenario, Indian J. Thorac. Cardiovasc. Surg., 35, 3, 10.1007/s12055-019-00789-z · DOI
  61. Santos, 2011, Biofilme em marca-passo artificial: ficção ou realidade, Arq. Bras. Cardiol., 97, e113, 10.1590/S0066-782X2011001400018 · DOI
  62. Saverina, 2023, From antibacterial to antibiofilm targeting: an emerging paradigm shift in the development of quaternary ammonium compounds (QACs), ACS Infect. Dis., 9, 394, 10.1021/acsinfecdis.2c00469 · DOI
  63. Schaible, 2012, Hypoxia Increases Antibiotic Resistance in Pseudomonas aeruginosa through Altering the Composition of Multidrug Efflux Pumps, Antimicrob. Agents Chemother., 56, 2114, 10.1128/AAC.05574-11 · DOI
  64. Shahrour, 2019, AMPs as anti-biofilm agents for human therapy and prophylaxis, 257
  65. Sharma, 2019, Antibiotics versus biofilm: an emerging battleground in microbial communities, Antimicrob. Resist. Infect. Control., 8, 76, 10.1186/s13756-019-0533-3 · DOI
  66. Singh, 2016, Penetration barrier contributes to bacterial biofilm-associated resistance against only select antibiotics, and exhibits genus-, strain- and antibiotic-specific differences, Pathog. Dis., 74, 10.1093/femspd/ftw056 · DOI
  67. Speziale, 2021, Monoclonal antibodies targeting surface-exposed and secreted proteins from staphylococci, Vaccines (Basel)., 9, 10.3390/VACCINES9050459 · DOI
  68. Tande, 2014, Prosthetic joint infection, Clin. Microbiol. Rev., 27, 302, 10.1128/CMR.00111-13 · DOI
  69. Townsend, 2020, CAUTI’s next top model - Model dependent Klebsiella biofilm inhibition by bacteriophages and antimicrobials, Biofilm, 2, 10.1016/j.bioflm.2020.100038 · DOI
  70. Toyofuku, 2016, Environmental factors that shape biofilm formation, Biosci. Biotechnol. Biochem., 80, 7, 10.1080/09168451.2015.1058701 · DOI · Paper page
  71. Tran, 2023, Debridement: technical considerations and treatment options for the interprofessional team, Adv. Skin. Wound Care, 36, 180, 10.1097/01.ASW.0000920660.07232.f7 · DOI
  72. Vazquez-Rodriguez, 2018, Microbial Competition of Rhodotorula mucilaginosa UANL-001L and E. coli increase biosynthesis of Non-Toxic Exopolysaccharide with Applications as a Wide-Spectrum Antimicrobial, Sci. Rep., 8, 798, 10.1038/s41598-017-17908-8 · DOI
  73. Wakharde, 2018, Anticancer drugs as antibiofilm agents in candida albicans: potential targets, Assay. Drug Dev. Technol., 16, 232, 10.1089/adt.2017.826 · DOI
  74. Wang, 2019, Regulatory mechanisms of the luxS/AI-2 system and bacterial resistance, Antimicrob. Agents Chemother., 63, 10.1128/AAC.01186-19 · DOI
  75. Wu, 2018, Hypoxia arising from concerted oxygen consumption by neutrophils and microorganisms in biofilms, Pathog. Dis., 76, 10.1093/femspd/fty043 · DOI
  76. Yang, 2017, Combination susceptibility testing of common antimicrobials in vitro and the effects of sub-MIC of antimicrobials on staphylococcus aureus biofilm formation, Front. Microbiol., 8, 10.3389/fmicb.2017.02125 · DOI
  77. Yasir, 2018, Action of antimicrobial peptides against bacterial biofilms, Mater. (Basel)., 11, 10.3390/ma11122468 · DOI
  78. Yin, 2013, Light based anti-infectives: ultraviolet C irradiation, photodynamic therapy, blue light, and beyond, Curr. Opin. Pharmacol., 13, 731, 10.1016/J.COPH.2013.08.009 · DOI
  79. Zimmermann, 2019, Clinically approved drugs inhibit the staphylococcus aureus multidrug norA efflux pump and reduce biofilm formation, Front. Microbiol., 10, 10.3389/fmicb.2019.02762 · DOI

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Authors
Grooters, K. E., Ku, J. C., Richter, D. M., Krinock, M. J., Minor, A., Li, P., Kim, A., Sawyer, R., & Li, Y.
Venue
Frontiers in Cellular and Infection Microbiology
Published
2024-01-19
Volume
14
ISSN
2235-2988
Cited by
156
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CoChat. (2026). Citation check: Strategies for combating antibiotic resistance in bacterial biofilms. https://app.cochat.ai/papers/10.3389/fcimb.2024.1352273
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Grooters, K. E., Ku, J. C., Richter, D. M., Krinock, M. J., Minor, A., Li, P., Kim, A., Sawyer, R., & Li, Y. (2024). Strategies for combating antibiotic resistance in bacterial biofilms. Frontiers in Cellular and Infection Microbiology. https://doi.org/10.3389/fcimb.2024.1352273