Liposomes used in the delivery of various antimicrobials to biofilm-producing infections: a systematic review

Document Type : Review Paper

Authors

1 Natural Products And Medicinal Plants Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran

2 Department of Medical Nanotechnology, School of Medicine, North Khorasan University of Medical Sciences, Bojnurd, Iran

3 Department of Medical Biotechnology, School of Medicine, North Khorasan University of Medical Sciences, Bojnurd, Iran

4 Department of Pathobiology and Laboratory Sciences, School of Medicine, North Khorasan University of Medical Sciences, Bojnurd, Iran

10.22038/nmj.2025.78800.1931

Abstract

Objective(s): Persistent clinical infections have driven extensive research to find effective solutions. Liposomes, known for their biocompatibility, versatility, targetability, and tunability, have emerged as a prominent drug delivery system. They enhance the delivery of contemporary antibiotics to resistant infections and facilitate the introduction of a wide range of novel antimicrobial agents.
Materials and Methods: This review adopts a systematic and thematic approach to encompass all studies involving liposomal antimicrobials for biofilm-producing infections. Original papers were retrieved from NCBI/PubMed using MeSH terms ‘liposome’, ‘antimicrobial’, and ‘biofilm’. An inductive qualitative thematic analysis was then conducted to identify the main themes and sub-themes. Themes supporting the primary objective and fundamentals were included, while those covered in previous reviews were excluded.
Results: Liposomes are an exceptional delivery system for treating clinical biofilm infections. They improve the delivery of contemporary hydrophobic antibiotics and enable the combinatorial introduction of natural and synthetic antimicrobials. Liposomes also serve as a suitable platform for controlled drug release, physicochemical modification, and surface functionalization with various biological ligands. Additionally, they allow for modifications that enhance adhesion to biotic and abiotic surfaces and support extended, prolonged drug release profiles with implants, scaffolds, and hydrogels.
Conclusion: Given their ease of manipulation and modulation, liposomes are anticipated to remain a long-standing drug delivery platform in future research focused on treating persistent infections with antimicrobials.

Keywords

References

  1. Alhajlan M, Alhariri M, Omri A. Efficacy and safety of liposomal clarithromycin and its effect on Pseudomonas aeruginosa virulence factors. Antimicrob Agents Chemother. 2013; 57(6): 2694-2704.
  2. Alipour M, Dorval C, Suntres ZE, Omri A. Bismuth-ethanedithiol incorporated in a liposome-loaded tobramycin formulation modulates the alginate levels in mucoid Pseudomonas aeruginosa. J Pharm Pharmacol. 2011; 63(8): 999-1007.
  3. Altube MJ, Martínez MM, Malheiros B, Maffía PC, Barbosa LR, Morilla MJ, et al. Fast biofilm penetration and anti-PAO1 activity of nebulized azithromycin in nanoarchaeosomes. Mol Pharm. 2019; 17(1): 70-83.
  4. Bandara H, Herpin M, Kolacny Jr D, Harb A, Romanovicz D, Smyth H. Incorporation of farnesol significantly increases the efficacy of liposomal ciprofloxacin against Pseudomonas aeruginosa biofilms in vitro. Mol Pharm. 2016; 13(8): 2760-2770.
  5. Cui H, Li W, Li C, Vittayapadung S, Lin L. Liposome containing cinnamon oil with antibacterial activity against methicillin-resistant Staphylococcus aureus biofilm. Biofouling. 2016; 32(2): 215-225.
  6. Finelli A, Burrows LL, DiCosmo FA, DiTizio V, Sinnadurai S, Oreopoulos DG, et al. Colonization-resistant antimicrobial-coated peritoneal dialysis catheters: evaluation in a newly developed rat model of persistent Pseudomonas aeruginosa peritonitis. Perit Dial Int. 2002; 22(1): 27-31.
  7. Marcos-Zambrano LJ, Gómez-Perosanz M, Escribano P, Zaragoza O, Bouza E, Guinea J. Biofilm production and antibiofilm activity of echinocandins and liposomal amphotericin B in echinocandin-resistant yeast species. Antimicrob Agents Chemother. 2016; 60(6): 3579-3586.
  8. Piri-Gharaghie T, Jegargoshe-Shirin N, Saremi-Nouri S, Khademhosseini S-h, Hoseinnezhad-Lazarjani E, Mousavi A, et al. Effects of Imipenem-containing Niosome nanoparticles against high prevalence methicillin-resistant Staphylococcus Epidermidis biofilm formed. Sci Rep. 2022; 12(1): 5140.
  9. Eladawy M, El-Mowafy M, El-Sokkary MMA, Barwa R. Effects of lysozyme, proteinase K, and cephalosporins on biofilm formation by clinical isolates of Pseudomonas aeruginosa. Interdiscip Perspect Infect Dis. 2020; 2020.
  10. Hedayati Ch M, Abolhassani Targhi A, Shamsi F, Heidari F, Salehi Moghadam Z, Mirzaie A, et al. Niosome‐encapsulated tobramycin reduced antibiotic resistance and enhanced antibacterial activity against multidrug‐resistant clinical strains of Pseudomonas aeruginosa. J Biomed Mater Res A. 2021; 109(6): 966-980.
  11. Barakat HS, Kassem MA, El-Khordagui LK, Khalafallah NM. Vancomycin-eluting niosomes: a new approach to the inhibition of staphylococcal biofilm on abiotic surfaces. AAPS PharmSciTech. 2014; 15: 1263-1274.
  12. Berti IR, Dell’Arciprete ML, Dittler ML, Minan A, de Mele MFL, Gonzalez M. Delivery of fluorophores by calcium phosphate-coated nanoliposomes and interaction with Staphylococcus aureus biofilms. Colloids Surf B Biointerfaces. 2016; 142: 214-222.
  13. Ramage G, Jose A, Sherry L, Lappin DF, Jones B, Williams C. Liposomal amphotericin B displays rapid dose-dependent activity against Candida albicans biofilms. Antimicrob Agents Chemother. 2013; 57(5): 2369-2371.
  14. Smistad G, Nguyen NB, Hegna IK, Sande SA. Influence of liposomal formulation variables on the interaction with Candida albicans in biofilm; a multivariate approach. J Liposome Res. 2011; 21(1): 9-16.
  15. Czuban M, Wulsten D, Wang L, Di Luca M, Trampuz A. Release of different amphotericin B formulations from PMMA bone cements and their activity against Candida biofilm. Colloids Surf B Biointerfaces. 2019; 183: 110406.
  16. Alipour M, Suntres ZE, Omri A. Importance of DNase and alginate lyase for enhancing free and liposome encapsulated aminoglycoside activity against Pseudomonas aeruginosa. J Antimicrob Chemother. 2009; 64(2): 317-325.
  17. Bandara H, Hewavitharana A, Shaw P, Smyth H, Samaranayake L. A novel, quorum sensor-infused liposomal drug delivery system suppresses Candida albicans biofilms. Int J Pharm. 2020; 578: 119096.
  18. Chan C, Burrows L, Deber C. Alginate as an auxiliary bacterial membrane: binding of membrane‐active peptides by polysaccharides. The Journal of peptide research. 2005; 65(3): 343-351.
  19. Tekintas Y, Demir-Dora D, Erac B, Erac Y, Yilmaz O, Aydemir SS, et al. Silencing acpP gene via antisense oligonucleotide-niosome complex in clinical Pseudomonas aeruginosa isolates. ResJMicrobiol. 2021; 172(4-5): 103834.
  20. Fang J-Y, Chou W-L, Lin C-F, Sung CT, Alalaiwe A, Yang S-C. Facile biofilm penetration of cationic liposomes loaded with DNase I/Proteinase K to eradicate Cutibacterium acnes for treating cutaneous and catheter infections. Int J Nanomedicine. 2021: 8121-8138.
  21. Sato Y, Unno Y, Miyazaki C, Ubagai T, Ono Y. Multidrug-resistant Acinetobacter baumannii resists reactive oxygen species and survives in macrophages. Sci Rep. 2019; 9(1): 17462.
  22. Gupta PV, Nirwane AM, Nagarsenker MS. Inhalable levofloxacin liposomes complemented with lysozyme for treatment of pulmonary infection in rats: effective antimicrobial and antibiofilm strategy. AAPS PharmSciTech. 2018; 19: 1454-1467.
  23. Meers P, Neville M, Malinin V, Scotto A, Sardaryan G, Kurumunda R, et al. Biofilm penetration, triggered release and in vivo activity of inhaled liposomal amikacin in chronic Pseudomonas aeruginosa lung infections. J Antimicrob Chemother. 2008; 61(4): 859-868.
  24. Kannan S, Solomon A, Krishnamoorthy G, Marudhamuthu M. Liposome encapsulated surfactant abetted copper nanoparticles alleviates biofilm mediated virulence in pathogenic Pseudomonas aeruginosa and MRSA. Sci Rep. 2021; 11(1): 1102.
  25. Alhariri M, Majrashi MA, Bahkali AH, Almajed FS, Azghani AO, Khiyami MA, et al. Efficacy of neutral and negatively charged liposome-loaded gentamicin on planktonic bacteria and biofilm communities. Int J Nanomedicine. 2017: 6949-6961.
  26. Angellotti G, Di Prima G, D’Agostino F, Peri E, Tricoli MR, Belfiore E, et al. Multicomponent Antibiofilm Lipid Nanoparticles as Novel Platform to Ameliorate Resveratrol Properties: Preliminary Outcomes on Fibroblast Proliferation and Migration. Int J Mol Sci. 2023; 24(9): 8382.
  27. Cottenye N, Cui Z-K, Wilkinson KJ, Barbeau J, Lafleur M. Interactions between non-phospholipid liposomes containing cetylpyridinium chloride and biofilms of Streptococcus mutans: modulation of the adhesion and of the biodistribution. Biofouling. 2013; 29(7): 817-827.
  28. Yamakami K, Tsumori H, Sakurai Y, Shimizu Y, Nagatoshi K, Sonomoto K. Sustainable inhibition efficacy of liposome-encapsulated nisin on insoluble glucan-biofilm synthesis by Streptococcus mutans. Pharm Biol. 2013; 51(2): 267-270.
  29. Gupta PV, Nirwane AM, Belubbi T, Nagarsenker MS. Pulmonary delivery of synergistic combination of fluoroquinolone antibiotic complemented with proteolytic enzyme: A novel antimicrobial and antibiofilm strategy. Nanomed Nanotechnol Biol Med. 2017; 13(7): 2371-84.
  30. Zhao Y, Dai X, Wei X, Yu Y, Chen X, Zhang X, et al. Near-infrared light-activated thermosensitive liposomes as efficient agents for photothermal and antibiotic synergistic therapy of bacterial biofilm. ACS Appl Mater Interfaces. 2018; 10(17): 14426-14437.
  31. Zhang L, Pornpattananangkul D, Hu C-M, Huang C-M. Development of nanoparticles for antimicrobial drug delivery. Curr Med Chem. 2010; 17(6): 585-594.
  32. Catuogno C, Jones MN. The antibacterial properties of solid supported liposomes on Streptococcus oralis biofilms. Int J Pharm. 2003; 257(1-2): 125-140.
  33. Ommen P, Hansen L, Hansen BK, Vu-Quang H, Kjems J, Meyer RL. Aptamer-targeted drug delivery for Staphylococcus aureus biofilm. Frontiers in Cellular and Infection Microbiology. 2022; 12: 814340.
  34. Shao H, Zhou J, Lin X, Zhou Y, Xue Y, Hong W, et al. Bio-inspired peptide-conjugated liposomes for enhanced planktonic bacteria killing and biofilm eradication. Biomaterials. 2023: 122183.
  35. Ahmed K, Gribbon P, Jones MN. The application of confocal microscopy to the study of liposome adsorption onto bacterial biofilms. J Liposome Res. 2002; 12(4): 285-300.
  36. Robinson AM, Creeth JE, Jones MN. The use of immunoliposomes for specific delivery of antimicrobial agents to oral bacteria immobilized on polystyrene. J Biomater Sci Polym Ed. 2000; 11(12): 1381-1393.
  37. Meng Y, Hou X, Lei J, Chen M, Cong S, Zhang Y, et al. Multi-functional liposomes enhancing target and antibacterial immunity for antimicrobial and anti-biofilm against methicillin-resistant Staphylococcus aureus. Pharm Res. 2016; 33: 763-775.
  38. Sudheesh M, Jain V, Shilakari G, Kohli D. Development and characterization of lectin-functionalized vesicular constructs bearing amphotericin B for bio-film targeting. Journal of drug targeting. 2009; 17(2): 148-158.
  39. Hallan SS, Marchetti P, Bortolotti D, Sguizzato M, Esposito E, Mariani P, et al. Design of nanosystems for the delivery of Quorum Sensing inhibitors: A preliminary study. Molecules. 2020; 25(23): 5655.
  40. Moghadas-Sharif N, Fazly Bazzaz BS, Khameneh B, Malaekeh-Nikouei B. The effect of nanoliposomal formulations on Staphylococcus epidermidis biofilm. Drug Development and Industrial Pharmacy. 2015; 41(3): 445-450.
  41. Mirzaie A, Peirovi N, Akbarzadeh I, Moghtaderi M, Heidari F, Yeganeh FE, et al. Preparation and optimization of ciprofloxacin encapsulated niosomes: A new approach for enhanced antibacterial activity, biofilm inhibition and reduced antibiotic resistance in ciprofloxacin-resistant methicillin-resistance Staphylococcus aureus. Bioorg Chem. 2020; 103: 104231.
  42. Rukavina Z, Klarić MŠ, Filipović-Grčić J, Lovrić J, Vanić Ž. Azithromycin-loaded liposomes for enhanced topical treatment of methicillin-resistant Staphyloccocus aureus (MRSA) infections. Int J Pharm. 2018; 553(1-2): 109-119.
  43. Dwivedi A, Mazumder A, Nasongkla N. Layer-by-layer nanocoating of antibacterial niosome on orthopedic implant. Int J Pharm. 2018; 547(1-2): 235-243.
  44. Xu M, Hu Y, Xiao Y, Zhang Y, Sun K, Wu T, et al. Near-infrared-controlled nanoplatform exploiting photothermal promotion of peroxidase-like and OXD-like activities for potent antibacterial and anti-biofilm therapies. ACS Appl Mater Interfaces. 2020; 12(45): 50260-50274.
  45. Fu Y-Y, Zhang L, Yang Y, Liu C-W, He Y-N, Li P, et al. Synergistic antibacterial effect of ultrasound microbubbles combined with chitosan-modified polymyxin B-loaded liposomes on biofilm-producing Acinetobacter baumannii. Int J Nanomedicine. 2019: 1805-1815.
  46. Ma D, Wu J. Biofilm mitigation by drug (gentamicin)-loaded liposomes promoted by pulsed ultrasound. The Journal of the Acoustical Society of America. 2016; 140(6): EL534-EL8.
  47. Plenagl N, Seitz BS, Duse L, Pinnapireddy SR, Jedelska J, Bruessler J, et al. Hypericin inclusion complexes encapsulated in liposomes for antimicrobial photodynamic therapy. Int J Pharm. 2019; 570: 118666.
  48. Rout B, Liu C-H, Wu W-C. Photosensitizer in lipid nanoparticle: a nano-scaled approach to antibacterial function. Sci Rep. 2017; 7(1): 7892.
  49. Wardlow R, Bing C, VanOsdol J, Maples D, Ladouceur-Wodzak M, Harbeson M, et al. Targeted antibiotic delivery using low temperature-sensitive liposomes and magnetic resonance-guided high-intensity focused ultrasound hyperthermia. Int J Hyperthermia. 2016; 32(3): 254-264.
  50. Wang D-Y, Yang G, Zhang X-X, van der Mei HC, Ren Y, Busscher HJ, et al. Proton-mediated burst of dual-drug loaded liposomes for biofilm dispersal and bacterial killing. J Control Release. 2022; 352: 460-471.
  51. Ma T, Shang B-C, Tang H, Zhou T-H, Xu G-L, Li H-L, et al. Nano-hydroxyapatite/chitosan/konjac glucomannan scaffolds loaded with cationic liposomal vancomycin: preparation, in vitro release and activity against Staphylococcus aureus biofilms. J Biomater Sci Polym Ed. 2011; 22(12): 1669-1681.
  52. Zhou T-H, Su M, Shang B-C, Ma T, Xu G-L, Li H-L, et al. Nano-hydroxyapatite/β-tricalcium phosphate ceramics scaffolds loaded with cationic liposomal ceftazidime: preparation, release characteristics in vitro and inhibition to Staphylococcus aureus biofilms. Drug development and industrial pharmacy. 2012; 38(11): 1298-1304.
  53. Ding T, Li T, Li J. Impact of curcumin liposomes with anti-quorum sensing properties against foodborne pathogens Aeromonas hydrophila and Serratia grimesii. Microb Pathog. 2018; 122: 137-143.
  54. Targhi AA, Moammeri A, Jamshidifar E, Abbaspour K, Sadeghi S, Lamakani L, et al. Synergistic effect of curcumin-Cu and curcumin-Ag nanoparticle loaded niosome: Enhanced antibacterial and anti-biofilm activities. Bioorg Chem. 2021; 115: 105116.
  55. Awad M, Barnes TJ, Joyce P, Thomas N, Prestidge CA. Liquid crystalline lipid nanoparticle promotes the photodynamic activity of gallium protoporphyrin against S. aureus biofilms. J Photochem Photobiol B: Biol. 2022; 232: 112474.
  56. Mahdiun F, Mansouri S, Khazaeli P, Mirzaei R. The effect of tobramycin incorporated with bismuth-ethanedithiol loaded on niosomes on the quorum sensing and biofilm formation of Pseudomonas aeruginosa. Microb Pathog. 2017; 107: 129-35.
  57. Zerillo L, Polvere I, Varricchio R, Madera JR, D’Andrea S, Voccola S, et al. Antibiofilm and repair activity of ozonated oil in liposome. Microb Biotechnol. 2022; 15(5): 1422-1433.
  58. Cutro AC, Coria MS, Bordon A, Rodriguez SA, Hollmann A. Antimicrobial properties of the essential oil of Schinus areira (Aguaribay) against planktonic cells and biofilms of S. aureus. Archives of Biochemistry and Biophysics. 2023: 109670.
  59. Pourhajibagher M, Partoazar A, Alaeddini M, Etemad-Moghadam S, Bahador A. Photodisinfection effects of silver sulfadiazine nanoliposomes doped-curcumin on Acinetobacter baumannii: a mouse model. Nanomedicine. 2020; 15(05): 437-452.
  60. Cressey P, Bronstein L-G, Benmahmoudi R, Rosilio V, Regeard C, Makky A. Novel liposome-like assemblies composed of phospholipid-porphyrin conjugates with photothermal and photodynamic activities against bacterial biofilms. Int J Pharm. 2022; 623: 121915.
  61. Sinsinwar S, Jayaraman A, Mahapatra SK, Vellingiri V. Anti-virulence properties of catechin-in-cyclodextrin-in-phospholipid liposome through down-regulation of gene expression in MRSA strains. Microb Pathog. 2022; 167: 105585.
  62. Alipour M, Suntres ZE, Lafrenie RM, Omri A. Attenuation of Pseudomonas aeruginosa virulence factors and biofilms by co-encapsulation of bismuth–ethanedithiol with tobramycin in liposomes. J Antimicrob Chemother. 2010; 65(4): 684-693.
  63. Blanchard JD, Elias V, Cipolla D, Gonda I, Bermudez LE. Effective treatment of Mycobacterium avium subsp. hominissuis and Mycobacterium abscessus species infections in macrophages, biofilm, and mice by using liposomal ciprofloxacin. Antimicrob Agents Chemother. 2018;62(10):10-128.
  64. Bhatia E, Sharma S, Jadhav K, Banerjee R. Combinatorial liposomes of berberine and curcumin inhibit biofilm formation and intracellular methicillin resistant Staphylococcus aureus infections and associated inflammation. J Mater Chem B. 2021; 9(3): 864-75.
  65. Cui H, Ma C, Lin L. Co-loaded proteinase K/thyme oil liposomes for inactivation of Escherichia coli O157: H7 biofilms on cucumber. Food Funct. 2016; 7(9): 4030-40.
  66. Wang DY, Yang G, van Der Mei HC, Ren Y, Busscher HJ, Shi L. Liposomes with Water as a pH‐Responsive Functionality for Targeting of Acidic Tumor and Infection Sites. Angew Chem. 2021; 133(32): 17855-60.
  67. Ellboudy NM, Elwakil BH, Shaaban MM, Olama ZA. Cinnamon Oil-Loaded Nanoliposomes with Potent Antibacterial and Antibiofilm Activities. Molecules. 2023; 28(11): 4492.
  68. Radaic A, Malone E, Kamarajan P, Kapila YL. Solid Lipid Nanoparticles Loaded with Nisin (SLN-Nisin) are More Effective Than Free Nisin as Antimicrobial, Antibiofilm, and Anticancer Agents. J Biomed Nanotechnol. 2022; 18(4): 1227-1235.
  69. Wang Z, Liu X, Peng Y, Su M, Zhu S, Pan J, et al. Platensimycin-encapsulated liposomes or micelles as biosafe nanoantibiotics exhibited strong antibacterial activities against methicillin-resistant Staphylococcus aureus infection in mice. Mol Pharm. 2020; 17(7): 2451-2462.
  70. Pu C, Tang W. The antibacterial and antibiofilm efficacies of a liposomal peptide originating from rice bran protein against Listeria monocytogenes. Food Funct. 2017; 8(11): 4159-4169.
  71. Jardeleza C, Thierry B, Rao S, Rajiv S, Drilling A, Miljkovic D, et al. An in vivo safety and efficacy demonstration of a topical liposomal nitric oxide donor treatment for Staphylococcus aureus biofilm–associated rhinosinusitis. Transl Res. 2015; 166(6): 683-692.
  72. Jardeleza C, Rao S, Thierry B, Gajjar P, Vreugde S, Prestidge CA, et al. Liposome-encapsulated ISMN: a novel nitric oxide-based therapeutic agent against Staphylococcus aureus biofilms. PLoS One. 2014; 9(3): e92117.
  73. Tsai M-J, Lin C-Y, Trousil J, Sung CT, Lee M-H, Fang J-Y, et al. Proteinase K/Retinoic Acid-Loaded Cationic Liposomes as Multifunctional Anti-Acne Therapy to Disorganize Biofilm and Regulate Keratinocyte Proliferation. Int J Nanomedicine. 2023: 3879-3896.
  74. Jones M, Kaszuba M, Hill K, Song Y-H, Creeth J. The use of phospholipid liposomes for targeting to oral and skin-associated bacteria. J Drug Target. 1994; 2(5): 381-389.
  75. Francolini I, Giansanti L, Piozzi A, Altieri B, Mauceri A, Mancini G. Glucosylated liposomes as drug delivery systems of usnic acid to address bacterial infections. Colloids Surf B Biointerfaces. 2019; 181: 632-638.
  76. Haque F, Sajid M, Cameotra SS, Battacharyya MS. Anti-biofilm activity of a sophorolipid-amphotericin B niosomal formulation against Candida albicans. Biofouling. 2017; 33(9): 768-779.
  77. Giordani B, Costantini PE, Fedi S, Cappelletti M, Abruzzo A, Parolin C, et al. Liposomes containing biosurfactants isolated from Lactobacillus gasseri exert antibiofilm activity against methicillin resistant Staphylococcus aureus strains. Eur J Pharm Biopharm. 2019; 139: 246-252.
  78. Rao Y, Sun Y, Li P, Xu M, Chen X, Wang Y, et al. Hypoxia-sensitive adjuvant loaded liposomes enhance the antimicrobial activity of azithromycin via phospholipase-triggered releasing for Pseudomonas aeruginosa biofilms eradication. Int J Pharm. 2022; 623: 121910.
  79. Hill KJ, Kaszuba M, Creeth JE, Jones MN. Reactive liposomes encapsulating a glucose oxidase-peroxidase system with antibacterial activity. Biochim Biophys Acta Biomembr. 1997; 1326(1): 37-46.
  80. Halwani M, Yebio B, Suntres ZE, Alipour M, Azghani AO, Omri A. Co-encapsulation of gallium with gentamicin in liposomes enhances antimicrobial activity of gentamicin against Pseudomonas aeruginosa. J Antimicrob Chemother. 2008; 62(6): 1291-1297.
  81. Halwani M, Hebert S, Suntres ZE, Lafrenie RM, Azghani AO, Omri A. Bismuth–thiol incorporation enhances biological activities of liposomal tobramycin against bacterial biofilm and quorum sensing molecules production by Pseudomonas aeruginosa. Int J Pharm. 2009; 373(1-2): 141-146.
  82. Ding T, Li T, Wang Z, Li J. Curcumin liposomes interfere with quorum sensing system of Aeromonas sobria and in silico analysis. Sci Rep. 2017; 7(1): 8612.
  83. Pinto RM, Monteiro C, Costa Lima SA, Casal S, Van Dijck P, Martins MCL, et al. N-acetyl-l-cysteine-loaded nanosystems as a promising therapeutic approach toward the eradication of Pseudomonas aeruginosa biofilms. ACS Applied Materials & Interfaces. 2021; 13(36): 42329-42343.
  84. Hou Y, Wang Z, Zhang P, Bai H, Sun Y, Duan J, et al. Lysozyme associated liposomal gentamicin inhibits bacterial biofilm. Int J Mol Sci. 2017; 18(4): 784.
  85. Zafari M, Adibi M, Chiani M, Bolourchi N, Barzi SM, Nosrati MSS, et al. Effects of cefazolin-containing niosome nanoparticles against methicillin-resistant Staphylococcus aureus biofilm formed on chronic wounds. JBiomedMater. 2021; 16(3): 035001.
  86. Bugli F, Posteraro B, Papi M, Torelli R, Maiorana A, Paroni Sterbini F, et al. In vitro interaction between alginate lyase and amphotericin B against Aspergillus fumigatus biofilm determined by different methods. Antimicrob Agents Chemother. 2013; 57(3): 1275-82.
  87. Kietrungruang K, Sookkree S, Sangboonruang S, Semakul N, Poomanee W, Kitidee K, et al. Ethanolic Extract Propolis-Loaded Niosomes Diminish Phospholipase B1, Biofilm Formation, and Intracellular Replication of Cryptococcus neoformans in Macrophages. Molecules. 2023; 28(17): 6224.
  88. Li C, Zhang X, Huang X, Wang X, Liao G, Chen Z. Preparation and characterization of flexible nanoliposomes loaded with daptomycin, a novel antibiotic, for topical skin therapy. International journal of nanomedicine. 2013: 1285-1292.
  89. Vanić Ž, Rukavina Z, Manner S, Fallarero A, Uzelac L, Kralj M, et al. Azithromycin-liposomes as a novel approach for localized therapy of cervicovaginal bacterial infections. Int J Nanomedicine. 2019: 5957-76.
  90. Luo Z, Lin Y, Zhou X, Yang L, Zhang Z, Liu Z, et al. Biomineral-binding liposomes with dual antibacterial effects for preventing and treating dental caries. BiomaterSci. 2023; 11(17): 5984-6000.
  91. Vyas S, Sihorkar V, Jain S. Mannosylated liposomes for bio-film targeting. Int J Pharm. 2007; 330(1-2): 6-13.
  92. Liu X-M, Zhang Y, Chen F, Khutsishvili I, Fehringer EV, Marky LA, et al. Prevention of Orthopedic Device-Associated Osteomyelitis Using Oxacillin-Containing Biomineral-Binding Liposomes. Pharm Res. 2012; 29(11): 3169-3179.
  93. Xie J, Meng Z, Han X, Li S, Ma X, Chen X, et al. Cholesterol microdomain enhances the biofilm eradication of antibiotic liposomes. Advanced healthcare materials. 2022; 11(8): 2101745.
  94. Ma D, Green AM, Willsey GG, Marshall JS, Wargo MJ, Wu J. Effects of acoustic streaming from moderate-intensity pulsed ultrasound for enhancing biofilm mitigation effectiveness of drug-loaded liposomes. J Acoust Soc Am. 2015; 138(2): 1043-1051.
  95. Munaweera I, Shaikh S, Maples D, Nigatu AS, Sethuraman SN, Ranjan A, et al. Temperature-sensitive liposomal ciprofloxacin for the treatment of biofilm on infected metal implants using alternating magnetic fields. Int J Hyperthermia. 2018; 34(2): 189-200.
  96. Dong D, Thomas N, Thierry B, Vreugde S, Prestidge CA, Wormald P-J. Distribution and inhibition of liposomes on Staphylococcus aureus and Pseudomonas aeruginosa biofilm. PLoS One. 2015; 10(6): e0131806.
  97. Sugano M, Morisaki H, Negishi Y, Endo-Takahashi Y, Kuwata H, Miyazaki T, et al. Potential effect of cationic liposomes on interactions with oral bacterial cells and biofilms. J Liposome Res. 2016; 26(2): 156-162.
  98. Kim HJ, Jones MN. The delivery of benzyl penicillin to Staphylococcus aureus biofilms by use of liposomes. J Liposome Res. 2004; 14(3-4): 123-139.
  99. Li D, Chen S, Dou H, Wu W, Liu Q, Zhang L, et al. Preparation of cefquinome sulfate cationic proliposome and evaluation of its efficacy on Staphylococcus aureus biofilm. Colloids Surf B Biointerfaces. 2019; 182: 110323.
  100. Messiaen A-S, Forier K, Nelis H, Braeckmans K, Coenye T. Transport of nanoparticles and tobramycin-loaded liposomes in Burkholderia cepacia complex biofilms. PLoS One. 2013; 8(11): e79220.
  101. Kluzek M, Oppenheimer-Shaanan Y, Dadosh T, Morandi MI, Avinoam O, Raanan C, et al. Designer liposomic nanocarriers are effective biofilm eradicators. ACS Nano. 2022; 16(10): 15792-15804.
  102. Jones MN. Use of liposomes to deliver bactericides to bacterial biofilms. Methods Enzymol. 2005; 391: 211-228. Elsevier.
  103. Metelkina O, Huck B, O'Connor JS, Koch M, Manz A, Lehr C-M, et al. Targeting extracellular lectins of Pseudomonas aeruginosa with glycomimetic liposomes. J Mater Chem B. 2022; 10(4): 537-548.
  104. Hemmingsen LM, Giordani B, Paulsen MH, Vanić Ž, Flaten GE, Vitali B, et al. Tailored anti-biofilm activity–Liposomal delivery for mimic of small antimicrobial peptide. Biomater Adv. 2023; 145: 213238.
  105. Patel KD, Mohid SA, Dutta A, Arichthota S, Bhunia A, Haldar D, et al. Synthesis and antibacterial study of cell-penetrating peptide conjugated trifluoroacetyl and thioacetyl lysine modified peptides. Eur J Med Chem. 2021; 219: 113447.
  106. Hu F, Zhou Z, Xu Q, Fan C, Wang L, Ren H, et al. A novel pH-responsive quaternary ammonium chitosan-liposome nanoparticles for periodontal treatment. Int J Biol Macromol. 2019; 129: 1113-1119.
  107. Mourtas S, Diamanti G, Foka A, Dracopoulos V, Klepetsanis P, Stamouli V, et al. Inhibition of bacterial attachment on surfaces by immobilization of tobramycin-loaded liposomes. J Biomed Nanotechnol. 2015; 11(12): 2186-2196.
  108. Tang H, Xu Y, Li G, You Y, Zhao X, Mei L, et al. Treatment of chronic osteomyelitis of rabbit with liposomal gentamicin-impregnated allogeneic cortical bone. Zhongguo xiu fu Chong Jian wai ke za zhi= Zhongguo Xiufu Chongjian Waike Zazhi= Chinese Journal of Reparative and Reconstructive Surgery. 2010; 24(4): 482-486.
  109. Eroğlu İ, Aslan M, Yaman Ü, Gultekinoglu M, Çalamak S, Kart D, et al. Liposome-based combination therapy for acne treatment. J Liposome Res. 2020; 30(3): 263-273.
  110. Hurler J, Sørensen KK, Fallarero A, Vuorela P, Škalko-Basnet N. Liposomes-in-hydrogel delivery system with mupirocin: in vitro antibiofilm studies and in vivo evaluation in mice burn model. Biomed Res Int. 2013; 2013.
  111. Hemmingsen LM, Giordani B, Pettersen AK, Vitali B, Basnet P, Škalko-Basnet N. Liposomes-in-chitosan hydrogel boosts potential of chlorhexidine in biofilm eradication in vitro. Carbohydr Polym. 2021; 262: 117939.
  112. Pugliese G, Favero MS. A Liposomal Hydrogel for the Prevention of Bacterial Adhesion to Catheters. Infect Control Hosp Epidemiol. 1999; 20(5): 368-.

 

Nanomedicine Journal
Volume 12, Issue 2
April 2025
Pages 153-180

Files

Share

How to cite

Statistics