Lipid and polymer nanoparticles for drug delivery to bacterial biofilms

Journal of Controlled Release

Volumn 190, Issue , 2014, Pages 607-623

  Forier, Katrien ^a   Raemdonck, Koen ^a   De Smedt, Stefaan C ^a   Demeester, Jo ^a   Coenye, Tom ^a   Braeckmans, Kevin ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Antibiotics; Biofilm; Drug delivery; Liposome; Nanomedicines; Polymer nanoparticles

Indexed keywords

ANTIBIOTICS; ANTIMICROBIAL AGENTS; BIOFILMS; CONTROLLED DRUG DELIVERY; DRUG DELIVERY; LIPOSOMES; MEDICAL NANOTECHNOLOGY; MICROORGANISMS; NANOPARTICLES; POLYMERS;

ANTI-MICROBIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; FUSOGENIC LIPOSOMES; LIPID NANOPARTICLES; POLYMER NANOPARTICLES; TRIGGERED DRUG RELEASE; TRIGGERED RELEASE;

TARGETED DRUG DELIVERY;

AMIKACIN; AMPHOTERICIN B CHOLESTEROL SULFATE; AMPHOTERICIN B LIPID COMPLEX; ANTIBIOTIC AGENT; BISMUTH; CEFTAZIDIME; CHLORHEXIDINE; CIPROFLOXACIN; CLARITHROMYCIN; DAPTOMYCIN; GENTAMICIN; GLUCOSE OXIDASE; LACTOPEROXIDASE; LIPID; LIPOQUIN; LIPOSOME; MEROPENEM; METRONIDAZOLE; NANOPARTICLE; NISIN; OXACILLIN; PENICILLIN G; POLYMER; POLYMYXIN B; PULMAQUIN; TEMOPORFIN; TOBRAMYCIN; TRICLOSAN; UNCLASSIFIED DRUG; VANCOMYCIN; ANTIINFECTIVE AGENT; DELAYED RELEASE FORMULATION; DRUG CARRIER;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BIOCOMPATIBILITY; CONTROLLED DRUG RELEASE; HUMAN; NANOENCAPSULATION; NONHUMAN; PRIORITY JOURNAL; BACTERIAL INFECTIONS; BACTERIUM; BIOFILM; CHEMISTRY; DELAYED RELEASE FORMULATION;

ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL INFECTIONS; BIOFILMS; DELAYED-ACTION PREPARATIONS; DRUG CARRIERS; HUMANS; LIPOSOMES; NANOPARTICLES; POLYMERS;

EID: 84906788755     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.03.055     Document Type: Review

References (130)

1. J.W. Costerton, G.G. Geesey, and K.J. Cheng How bacteria stick Sci. Am. 238 1978 86
2. L. Hall-Stoodley, and P. Stoodley Evolving concepts in biofilm infections Cell. Microbiol. 11 2009 1034 1043
3. M.S.P.B.D. Aparna, and S. Yadav Biofilms: microbes and disease Braz. J. Infect. Dis. 12 2008 526 530
4. J.L. del Pozo, and R. Patel The challenge of treating biofilm-associated bacterial infections Clin. Pharmacol. Ther. 82 2007 204 209 (Pubitemid 47075342)
5. M.R. Parsek, and P.K. Singh Bacterial biofilms: an emerging link to disease pathogenesis Annu. Rev. Microbiol. 57 2003 677 701 (Pubitemid 37392958)
6. J.W. Costerton, Z. Lewandowski, D.E. Caldwell, D.R. Korber, and H.M. Lappinscott Microbial biofilms Annu. Rev. Microbiol. 49 1995 711 745
7. P. Stoodley, K. Sauer, D.G. Davies, and J.W. Costerton Biofilms as complex differentiated communities Annu. Rev. Microbiol. 56 2002 187 209 (Pubitemid 35217453)
8. B.L. Bassler How bacteria talk to each other: regulation of gene expression by quorum sensing Curr. Opin. Microbiol. 2 1999 582 587
9. P. Williams, K. Winzer, W.C. Chan, and M. Camara Look who's talking: communication and quorum sensing in the bacterial world Philos. Trans. R. Soc. B 362 2007 1119 1134 (Pubitemid 47075145)
10. C.D. Sifri Quorum sensing: bacteria talk sense Clin. Infect. Dis. 47 2008 1070 1076
11. P.L. Phillips, R.D. Wolcott, J.I. Fletcher, and G.S. Schultz Biofilms made easy Wounds Int. 1 2010 s1.1 s1.6
12. T. Bjarnsholt, M. Alhede, M. Alhede, S.R. Eickhardt-Sørensen, C. Moser, M. Kühl, P.∅. Jensen, and N. Høiby The in vivo biofilm Trends Microbiol. 21 2013 466 474
13. J.C. Nickel, I. Ruseska, J.B. Wright, and J.W. Costerton Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material Antimicrob. Agents Chemother. 27 1985 619 624 (Pubitemid 15097672)
14. K. Lewis Riddle of biofilm resistance Antimicrob. Agents Chemother. 45 2001 999 1007 (Pubitemid 32230975)
15. K. Lewis Multidrug tolerance of biofilms and persister cells Curr. Top. Microbiol. Immunol. 322 2008 107 131
16. E.T. Jensen, A. Kharazmi, K. Lam, J.W. Costerton, and N. Høiby Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms Infect. Immun. 58 1990 2383 2385 (Pubitemid 20212322)
17. J.W. Costerton, P.S. Stewart, and E.P. Greenberg Bacterial biofilms: a common cause of persistent infections Science 284 1999 1318 1322 (Pubitemid 29289651)
18. J.L. Pace, M.E. Rupp, and R.G. Finch Biofilms, Infection and Antimicrobial Therapy 2006 CRC Press Boca Raton 501
19. C.A. Fux, J.W. Costerton, P.S. Stewart, and P. Stoodley Survival strategies of infectious biofilms Trends Microbiol. 13 2005 34 40 (Pubitemid 40082395)
20. N. Hoiby, T. Bjarnsholt, M. Givskov, S. Molin, and O. Ciofu Antibiotic resistance of bacterial biofilms Int. J. Antimicrob. Agents 35 2010 322 332
21. M. Fauvart, V.N. De Groote, and J. Michiels Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies J. Med. Microbiol. 60 2011 699 709
22. S. Parveen, R. Misra, and S.K. Sahoo Nanoparticles: a boon to drug delivery, therapeutics, diagnostics and imaging Nanomedicine 8 2012 147 166
23. A. Akbarzadeh, R. Rezaei-Sadabady, S. Davaran, S.W. Joo, N. Zarghami, Y. Hanifehpour, M. Samiei, M. Kouhi, and K. Nejati-Koshki Liposome: classification, preparation, and applications Nanoscale Res. Lett. 8 2013
24. L.C. Gomes-da-Silva, N.A. Fonseca, V. Moura, M.C. Pedroso de Lima, S. Simões, and J.N. Moreira Lipid-based nanoparticles for siRNA delivery in cancer therapy: paradigms and challenges Acc. Chem. Res. 45 2012 1163 1171
25. D. Nicolosi, M. Scalia, V.M. Nicolosi, and R. Pignatello Encapsulation in fusogenic liposomes broadens the spectrum of action of vancomycin against Gram-negative bacteria Int. J. Antimicrob. Agents 35 2010 553 558
26. M. Vidal, and D. Hoekstra In vitro fusion of reticulocyte endocytic vesicles with liposomes J. Biol. Chem. 270 1995 17823 17829
27. G. Cevc How membrane chain-melting phase-transition temperature is affected by the lipid chain asymmetry and degree of unsaturation: an effective chain-length model Biochemistry 30 1991 7186 7193
28. P.L. Chong, and D. Choate Calorimetric studies of the effects of cholesterol on the phase transition of C(18):C(10) phosphatidylcholine Biophys. J. 55 1989 551 556 (Pubitemid 19073742)
29. K. Hadinoto, and W.S. Cheow Nano-antibiotics in chronic lung infection therapy against Pseudomonas aeruginosa Colloids Surf. B: Biointerfaces 116 2014 772 785
30. T.N. Günday, A.E. Türeli, and M. Schneider Inhalable antibiotic nanoformulations against P. aeruginosa Drug Deliv. Lett. 2014 10.2174/2210303104666140222002101 (epub ahead of print)
31. C. Beaulac, S. Clement-Major, J. Hawari, and J. Lagace Eradication of mucoid Pseudomonas aeruginosa with fluid liposome-encapsulated tobramycin in an animal model of chronic pulmonary infection Antimicrob. Agents Chemother. 40 1996 665 669
32. C. Beaulac, S. Sachetelli, and J. Lagace In vitro bactericidal evaluation of a low phase transition temperature liposomal tobramycin formulation as a dry powder preparation against Gram negative and Gram positive bacteria J. Liposome Res. 9 1999 301 312 (Pubitemid 29439397)
33. C. Beaulac, S. Sachetelli, and J. Lagace In-vitro bactericidal efficacy of sub-MIC concentrations of liposome-encapsulated antibiotic against gram-negative and gram-positive bacteria J. Antimicrob. Chemother. 41 1998 35 41 (Pubitemid 28064248)
34. S. Sachetelli, H. Khalil, T. Chen, C. Beaulac, S. Senechal, and J. Lagace Demonstration of a fusion mechanism between a fluid bactericidal liposomal formulation and bacterial cells Biochim. Biophys. Acta Biomembr. 1463 2000 254 266 (Pubitemid 30081785)
35. Z. Drulis-Kawa, J. Gubernator, A. Dorotkiewicz-Jach, W. Doroszkiewicz, and A. Kozubek In vitro antimicrobial activity of liposomal meropenem against Pseudomonas aeruginosa strains Int. J. Pharm. 315 2006 59 66 (Pubitemid 43674108)
36. M. Halwani, C. Mugabe, A.O. Azghani, R.M. Lafrenie, A. Kumar, and A. Omri Bactericidal efficacy of liposomal aminoglycosides against Burkholderia cenocepacia J. Antimicrob. Chemother. 60 2007 760 769 (Pubitemid 47434253)
37. C. Mugabe, M. Halwani, A.O. Azghani, R.M. Lafrenie, and A. Omri Mechanism of enhanced activity of liposome-entrapped aminoglycosides against resistant strains of Pseudomonas aeruginosa Antimicrob. Agents Chemother. 50 2006 2016 2022 (Pubitemid 43807520)
38. C. Li, X.L. Zhang, X.L. Huang, X.Y. Wang, G.J. Liao, and Z.B. Chen Preparation and characterization of flexible nanoliposomes loaded with daptomycin, a novel antibiotic, for topical skin therapy Int. J. Nanomed. 8 2013 1285 1292
39. Z. Drulis-Kawa, A. Dorotkiewicz-Jach, J. Gubernator, G. Gula, T. Bocer, and W. Doroszkiewicz The interaction between Pseudomonas aeruginosa cells and cationic PC:Chol:DOTAP liposomal vesicles versus outer-membrane structure and envelope properties of bacterial cell Int. J. Pharm. 367 2009 211 219
40. M.C. Walters, F. Roe, A. Bugnicourt, M.J. Franklin, and P.S. Stewart Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin Antimicrob. Agents Chemother. 47 2003 317 323 (Pubitemid 36070381)
41. B.E. Hunt, A. Weber, A. Berger, B. Ramsey, and A.L. Smith Macromolecular mechanisms of sputum inhibition of tobramycin activity Antimicrob. Agents Chemother. 39 1995 34 39
42. C. Mugabe, A.O. Azghani, and A. Omri Liposome-mediated gentamicin delivery: development and activity against resistant strains of Pseudomonas aeruginosa isolated from cystic fibrosis patients J. Antimicrob. Chemother. 55 2005 269 271 (Pubitemid 40331158)
43. M.C. Nacucchio, M.J. Bellora, D.O. Sordelli, and M. D'Aquino Enhanced liposome-mediated activity of piperacillin against staphylococci Antimicrob. Agents Chemother. 27 1985 137 139 (Pubitemid 15198171)
44. M. Alipour, Z.E. Suntres, M. Halwani, A.O. Azghani, and A. Omri Activity and interactions of liposomal antibiotics in presence of polyanions and sputum of patients with cystic fibrosis PLoS One 4 2009 e5724
45. M. Halwani, S. Blomme, Z.E. Suntres, M. Alipour, A.O. Azghani, A. Kumar, and A. Omri Liposomal bismuth-ethanedithiol formulation enhances antimicrobial activity of tobramycin Int. J. Pharm. 358 2008 278 284
46. M. Halwani, B. Yebio, Z.E. Suntres, M. Alipour, A.O. Azghani, and A. Omri Co-encapsulation of gallium with gentamicin in liposomes enhances antimicrobial activity of gentamicin against Pseudomonas aeruginosa J. Antimicrob. Chemother. 62 2008 1291 1297
47. M. Alipour, C. Dorval, Z.E. Suntres, and A. Omri Bismuth-ethanedithiol incorporated in a liposome-loaded tobramycin formulation modulates the alginate levels in mucoid Pseudomonas aeruginosa J. Pharm. Pharmacol. 63 2011 999 1007
48. M. Alipour, Z.E. Suntres, R.M. Lafrenie, and A. Omri Attenuation of Pseudomonas aeruginosa virulence factors and biofilms by co-encapsulation of bismuth-ethanedithiol with tobramycin in liposomes J. Antimicrob. Chemother. 65 2010 684 693
49. M. Halwani, S. Hebert, Z.E. Suntres, R.M. Lafrenie, A.O. Azghani, and A. Omri Bismuth-thiol incorporation enhances biological activities of liposomal tobramycin against bacterial biofilm and quorum sensing molecules production by Pseudomonas aeruginosa Int. J. Pharm. 373 2009 141 146
50. M. Alhariri, and A. Omri Efficacy of liposomal bismuth-ethanedithiol- loaded tobramycin after intratracheal administration in rats with pulmonary Pseudomonas aeruginosa infection Antimicrob. Agents Chemother. 57 2013 569 578
51. P. Meers, M. Neville, V. Malinin, A.W. Scotto, G. Sardaryan, R. Kurumunda, C. Mackinson, G. James, S. Fisher, and W.R. Perkins Biofilm penetration, triggered release and in vivo activity of inhaled liposomal amikacin in chronic Pseudomonas aeruginosa lung infections J. Antimicrob. Chemother. 61 2008 859 868 (Pubitemid 351426071)
52. M. Alhajlan, M. Alhariri, and A. Omri Efficacy and safety of liposomal clarithromycin and its effect on Pseudomonas aeruginosa virulence factors Antimicrob. Agents Chemother. 57 2013 2694 2704
53. C.-T. Zhu, Y.-Q. Xu, J. Shi, J. Li, and J. Ding Liposome combined porous beta-TCP scaffold: preparation, characterization, and anti-biofilm activity Drug Deliv. 17 2010 391 398
54. T.H. Zhou, M. Su, B.C. Shang, T. Ma, G.L. Xu, H.L. Li, Q.H. Chen, W. Sun, and Y.Q. Xu Nano-hydroxyapatite/beta-tricalcium phosphate ceramics scaffolds loaded with cationic liposomal ceftazidime: preparation, release characteristics in vitro and inhibition to Staphylococcus aureus biofilms Drug Dev. Ind. Pharm. 38 2012 1298 1304
55. T. Ma, B.-C. Shang, H. Tang, T.-H. Zhou, G.-L. Xu, H.-L. Li, Q.-H. Chen, and Y.-Q. Xu 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. 22 2011 1669 1681
56. X.M. Liu, Y.J. Zhang, F. Chen, I. Khutsishvili, E.V. Fehringer, L.A. Marky, K.W. Bayles, and D. Wang Prevention of orthopedic device-associated osteomyelitis using oxacillin-containing biomineral-binding liposomes Pharm. Res. 29 2012 3169 3179
57. K. Yamakami, H. Tsumori, Y. Sakurai, Y. Shimizu, K. Nagatoshi, and K. Sonomoto Sustainable inhibition efficacy of liposome-encapsulated nisin on insoluble glucan-biofilm synthesis by Streptococcus mutans Pharm. Biol. 51 2013 267 270
58. F. Chen, X.M. Liu, K.C. Rice, X. Li, F. Yu, R.A. Reinhardt, K.W. Bayles, and D. Wang Tooth-binding micelles for dental caries prevention Antimicrob. Agents Chemother. 53 2009 4898 4902
59. V. DiTizio, G.W. Ferguson, M.W. Mittelman, A.E. Khoury, A.W. Bruce, and F. DiCosmo A liposomal hydrogel for the prevention of bacterial adhesion to catheters Biomaterials 19 1998 1877 1884 (Pubitemid 28519970)
60. J.F. Marier, J. Lavigne, and M.P. Ducharme Pharmacokinetics and efficacies of liposomal and conventional formulations of tobramycin after intratracheal administration in rats with pulmonary Burkholdefia cepacia infection Antimicrob. Agents Chemother. 46 2002 3776 3781 (Pubitemid 35403251)
61. H. Tang, Y. Xu, T. Zheng, G. Li, Y. You, M. Jiang, J. Li, and J. Ding Treatment of osteomyelitis by liposomal gentamicin-impregnated calcium sulfate Arch. Orthop. Trauma Surg. 129 2009 1301 1308
62. J.P. Clancy, L. Dupont, M.W. Konstan, J. Billings, S. Fustik, C.H. Goss, J. Lymp, P. Minic, A.L. Quittner, R.C. Rubenstein, K.R. Young, L. Saiman, J.L. Burns, J.R.W. Govan, B. Ramsey, R. Gupta, and f.t.A.S. Group Phase II studies of nebulised Arikace in CF patients with Pseudomonas aeruginosa infection Thorax 68 2013 818 825
63. P. Bruinenberg, J.D. Blanchard, D.C. Cipolla, F. Dayton, S. Mudumba, and I. Gonda Inhaled liposomal ciprofloxacin: once a day management of respiratory infections Respir. Drug Deliv. 1 2010 73 82
64. A.S. Messiaen, K. Forier, H. Nelis, K. Braeckmans, and T. Coenye Transport of nanoparticles and tobramycin-loaded liposomes in Burkholderia cepacia complex biofilms PLoS One 8 2013 e79220
65. J. Gubernator, Z. Druis-Kawa, A. Dorotkiewicz-Jach, W. Doroszkiewicz, and A. Kozubek In vitro antimicrobial activity of liposomes containing ciprofloxacin, meropenem and gentamicin against gram-negative clinical bacterial strains Lett. Drug Des. Discov. 4 2007 297 304 (Pubitemid 46708895)
66. J. Hernández-Borrell, and M.T. Montero Does ciprofloxacin interact with neutral bilayers? An aspect related to its antimicrobial activity Int. J. Pharm. 252 2003 149 157 (Pubitemid 36126623)
67. J.L. Kadurugamuwa, J.S. Lam, and T.J. Beveridge Interaction of gentamicin with the A band and B band lipopolysaccharides of Pseudomonas aeruginosa and its possible lethal effect Antimicrob. Agents Chemother. 37 1993 715 721 (Pubitemid 23096867)
68. M. Alipour, Z.E. Suntres, and A. Omri Importance of DNase and alginate lyase for enhancing free and liposome encapsulated aminoglycoside activity against Pseudomonas aeruginosa J. Antimicrob. Chemother. 64 2009 317 325
69. Z. Drulis-Kawa, and A. Dorotkiewicz-Jach Liposomes as delivery systems for antibiotics Int. J. Pharm. 387 2010 187 198
70. C. Mugabe, A.O. Azghani, and A. Omri Preparation and characterization of dehydration-rehydration vesicles loaded with aminoglycoside and macrolide antibiotics Int. J. Pharm. 307 2006 244 250 (Pubitemid 41820421)
71. K.J. Hill, M. Kaszuba, J.E. Creeth, and M.N. Jones Reactive liposomes encapsulating a glucose oxidase-peroxidase system with antibacterial activity Biochim. Biophys. Acta Biomembr. 1326 1997 37 46 (Pubitemid 27226808)
72. M.N. Jones, K.J. Hill, M. Kaszuba, and J.E. Creeth Antibacterial reactive liposomes encapsulating coupled enzyme systems Int. J. Pharm. 162 1998 107 117 (Pubitemid 28166096)
73. H.J. Kim, and M.N. Jones The delivery of benzyl penicillin to Staphylococcus aureus biofilms by use of liposomes J. Liposome Res. 14 2004 123 139 (Pubitemid 40052466)
74. S. Nguyen, M. Hiorth, M. Rykke, and G. Smistad Polymer coated liposomes for dental drug delivery - Interactions with parotid saliva and dental enamel Eur. J. Pharm. Sci. 50 2013 78 85
75. M.N. Jones, M. Kaszuba, M.D. Reboiras, I.G. Lyle, K.J. Hill, Y.H. Song, S.W. Wilmot, and J.E. Creeth The targeting of phospholipid liposomes to bacteria Biochim. Biophys. Acta Biomembr. 1196 1994 57 64 (Pubitemid 24372345)
76. N.M. Sanderson, and M.N. Jones Targeting of cationic liposomes to skin-associated bacteria Pestic. Sci. 46 1996 255 261 (Pubitemid 126759762)
77. N.M. Sanderson, B.Q. Guo, A.E. Jacob, P.S. Handley, J.G. Cunniffe, and M.N. Jones The interaction of cationic liposomes with the skin-associated bacterium Staphylococcus epidermidis: effects of ionic strength and temperature Biochim. Biophys. Acta Biomembr. 1283 1996 207 214 (Pubitemid 26290715)
78. M.N. Jones, Y.H. Song, M. Kaszuba, and M.D. Reboiras The interaction of phospholipid liposomes with bacteria and their use in the delivery of bactericides J. Drug Target. 5 1997 25 34 (Pubitemid 28057017)
79. H.J. Kim, E.L.M. Gias, and M.N. Jones The adsorption of cationic liposomes to Staphylococcus aureus biofilms Colloids Surf. A Physicochem. Eng. Asp. 149 1999 561 570 (Pubitemid 29132720)
80. A.M. Robinson, M. Bannister, J.E. Creeth, and M.N. Jones The interaction of phospholipid liposomes with mixed bacterial biofilms and their use in the delivery of bactericide Colloids Surf. A Physicochem. Eng. Asp. 186 2001 43 53 (Pubitemid 32496529)
81. A.M. Robinson, J.E. Creeth, and M.N. Jones The use of immunoliposomes for specific delivery of antimicrobial agents to oral bacteria immobilized on polystyrene J. Biomater. Sci. Polym. Ed. 11 2000 1381 1393 (Pubitemid 32208317)
82. A.M. Robinson, J.E. Creeth, and M.N. Jones The specificity and affinity of immunoliposome targeting to oral bacteria Biochim. Biophys. Acta Biomembr. 1369 1998 278 286 (Pubitemid 28132865)
83. M. Kaszuba, A.M. Robinson, Y.H. Song, J.E. Creeth, and M.N. Jones The visualisation of the targeting of phospholipid liposomes to bacteria Colloids Surf. B: Biointerfaces 8 1997 321 332 (Pubitemid 27250322)
84. M. Kaszuba, I.G. Lyle, and M.N. Jones The targeting of lectin-bearing liposomes to skin-associated bacteria Colloids Surf. B: Biointerfaces 4 1995 151 158
85. S.P. Vyas, V. Sihorkar, and P.K. Dubey Preparation, characterization and in vitro antimicrobial activity of metronidazole bearing lectinized liposomes for intra-periodontal pocket delivery Pharmazie 56 2001 554 560 (Pubitemid 32634693)
86. M.N. Jones, M. Kaszuba, K.J. Hill, Y.H. Song, and J.E. Creeth The use of phospholipid liposomes for targeting to oral and skin-associated bacteria J. Drug Target. 2 1994 381 389
87. M.N. Jones, S.E. Francis, F.J. Hutchinson, P.S. Handley, and I.G. Lyle Targeting and delivery of bactericide to adsorbed oral bacteria by use of proteoliposomes Biochim. Biophys. Acta Biomembr. 1147 1993 251 261 (Pubitemid 23116046)
88. K. Yang, B. Gitter, R. Rüger, V. Albrecht, G.D. Wieland, and A. Fahr Wheat germ agglutinin modified liposomes for the photodynamic inactivation of bacteria † Photochem. Photobiol. 88 2012 548 556
89. K. Raemdonck, K. Braeckmans, J. Demeester, and S.C. De Smedt Merging the best of both worlds: hybrid lipid-enveloped matrix nanocomposites in drug delivery Chem. Soc. Rev. 43 2014 444 472
90. K. Hadinoto, A. Sundaresan, and W.S. Cheow Lipid-polymer hybrid nanoparticles as a new generation therapeutic delivery platform: a review Eur. J. Pharm. Biopharm. 85 2013 427 443
91. F. Danhier, E. Ansorena, J.M. Silva, R. Coco, A. Le Breton, and V. Préat PLGA-based nanoparticles: an overview of biomedical applications J. Control. Release 161 2012 505 522
92. Y. Fang, M.M. Lou, B. Li, G.L. Xie, F. Wang, L.X. Zhang, and Y.C. Luo Characterization of Burkholderia cepacia complex from cystic fibrosis patients in China and their chitosan susceptibility World J. Microbiol. Biotechnol. 26 2010 443 450
93. S.M. Abdelghany, D.J. Quinn, R.J. Ingram, B.F. Gilmore, R.F. Donnelly, C.C. Taggart, and C.J. Scott Gentamicin-loaded nanoparticles show improved antimicrobial effects towards Pseudomonas aeruginosa infection Int. J. Nanomed. 7 2012 4053 4063
94. W.S. Cheow, M.W. Chang, and K. Hadinoto The roles of lipid in anti-biofilm efficacy of lipid-polymer hybrid nanoparticles encapsulating antibiotics Colloids Surf. A Physicochem. Eng. Asp. 389 2011 158 165
95. W.S. Cheow, M.W. Chang, and K. Hadinoto Antibacterial efficacy of inhalable antibiotic-encapsulated biodegradable polymeric nanoparticles against E. coli biofilm cells J. Biomed. Nanotechnol. 6 2010 391 403
96. W.S. Cheow, M.W. Chang, and K. Hadinoto Antibacterial efficacy of inhalable levofloxacin-loaded polymeric nanoparticles against E. coli biofilm cells: the effect of antibiotic release profile Pharm. Res. 27 2010 1597 1609
97. E.I. Rabea, M.E.T. Badawy, C.V. Stevens, G. Smagghe, and W. Steurbaut Chitosan as antimicrobial agent: applications and mode of action Biomacromolecules 4 2003 1457 1465 (Pubitemid 37455555)
98. L.E. Chavez de Paz, A. Resin, K.A. Howard, D.S. Sutherland, and P.L. Wejse Antimicrobial effect of chitosan nanoparticles on Streptococcus mutans biofilms Appl. Environ. Microbiol. 77 2011 3892 3895
99. S.P. Chakraborty, S.K. Sahu, P. Pramanik, and S. Roy In vitro antimicrobial activity of nanoconjugated vancomycin against drug resistant Staphylococcus aureus Int. J. Pharm. 436 2012 659 676
100. S.P. Chakraborty, S.K. Sahu, S.K. Mahapatra, S. Santra, M. Bal, S. Roy, and P. Pramanik Nanoconjugated vancomycin: new opportunities for the development of anti-VRSA agents Nanotechnology 21 2010
101. W.S. Cheow, and K. Hadinoto Enhancing encapsulation efficiency of highly water-soluble antibiotic in poly(lactic-co-glycolic acid) nanoparticles: modifications of standard nanoparticle preparation methods Colloids Surf. A Physicochem. Eng. Asp. 370 2010 79 86
102. F. Ungaro, I. d'Angelo, C. Coletta, R. d'Emmanuele di Villa Bianca, R. Sorrentino, B. Perfetto, M.A. Tufano, A. Miro, M.I. La Rotonda, and F. Quaglia Dry powders based on PLGA nanoparticles for pulmonary delivery of antibiotics: modulation of encapsulation efficiency, release rate and lung deposition pattern by hydrophilic polymers J. Control. Release 157 2012 149 159
103. W.S. Cheow, and K. Hadinoto Factors affecting drug encapsulation and stability of lipid-polymer hybrid nanoparticles Colloids Surf. B: Biointerfaces 85 2011 214 220
104. W.S. Cheow, and K. Hadinoto Green preparation of antibiotic nanoparticle complex as potential anti-biofilm therapeutics via self-assembly amphiphile-polyelectrolyte complexation with dextran sulfate Colloids Surf. B: Biointerfaces 92 2012 55 63
105. A. Iannitelli, R. Grande, A. Di Stefano, M. Di Giulio, P. Sozio, L.J. Bessa, S. Laserra, C. Paolini, F. Protasi, and L. Cellini Potential antibacterial activity of carvacrol-loaded poly(DL-lactide-co-glycolide) (PLGA) nanoparticles against microbial biofilm Int. J. Mol. Sci. 12 2011 5039 5051
106. W.S. Cheow, and K. Hadinoto Lipid-polymer hybrid nanoparticles with rhamnolipid-triggered release capabilities as anti-biofilm drug delivery vehicles Particuology 10 2012 327 333
107. M.N. Jones, and M. Kaszuba Polyhydroxy-mediated interactions between liposomes and bacterial biofilms Biochim. Biophys. Acta Biomembr. 1193 1994 48 54 (Pubitemid 24234177)
108. E. Yoshihara, and T. Nakae Cytolytic activity of liposomes containing stearylamine Biochim. Biophys. Acta Biomembr. 854 1986 93 101 (Pubitemid 16165481)
109. J.H. Senior, K.R. Trimble, and R. Maskiewicz Interaction of positively-charged liposomes with blood: implications for their application in vivo Biochim. Biophys. Acta Biomembr. 1070 1991 173 179
110. I.J. Goldstein, C.M. Reichert, A. Misaki, and P.A.J. Gorin An "extension" of the carbohydrate binding specificity of concanavalin A Biochim. Biophys. Acta Protein Struct. 317 1973 500 504
111. J.F. Kennedy, P.M.G. Palva, M.T.S. Corella, M.S.M. Cavalcanti, and L.C.B.B. Coelho Lectins, versatile proteins of recognition: a review Carbohydr. Polym. 26 1995 219 230
112. M. Strathmann, J. Wingender, and H.C. Flemming Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa J. Microbiol. Methods 50 2002 237 248 (Pubitemid 34603268)
113. I.J. Goldstein, and C.E. Hayes The Lectins: carbohydrate-binding proteins of plants and animals R.S. Tipson, H. Derek, Advances in Carbohydrate Chemistry and Biochemistry 1978 Academic Press 127 340
114. S. Bibi, E. Lattmann, A.R. Mohammed, and Y. Perrie Trigger release liposome systems: local and remote controlled delivery? J. Microencapsul. 29 2012 262 276
115. E. Guiot, P. Georges, A. Brun, M.P. Fontaine-Aupart, M.N. Bellon-Fontaine, and R. Briandet Heterogeneity of diffusion inside microbial biofilms determined by fluorescence correlation spectroscopy under two-photon excitation Photochem. Photobiol. 75 2002 570 578
116. P.S. Stewart Diffusion in biofilms J. Bacteriol. 185 2003 1485 1491 (Pubitemid 36245948)
117. K.K. Jefferson, D.A. Goldmann, and G.B. Pier Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms Antimicrob. Agents Chemother. 49 2005 2467 2473 (Pubitemid 40734481)
118. S.A. Rani, B. Pitts, and P.S. Stewart Rapid diffusion of fluorescent tracers into Staphylococcus epidermidis biofilms visualized by time lapse microscopy Antimicrob. Agents Chemother. 49 2005 728 732 (Pubitemid 40175686)
119. S. Takenaka, B. Pitts, H.M. Trivedi, and P.S. Stewart Diffusion of macromolecules in model oral biofilms Appl. Environ. Microbiol. 75 2009 1750 1753
120. N. Bagge, M. Schuster, M. Hentzer, O. Ciofu, M. Givskov, E.P. Greenberg, and N. Høiby Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-Lactamase and alginate production Antimicrob. Agents Chemother. 48 2004 1175 1187 (Pubitemid 38405471)
121. K. Ahmed, P. Gribbon, and M.N. Jones The application of confocal microscopy to the study of liposome adsorption onto bacterial biofilms J. Liposome Res. 12 2002 285 300 (Pubitemid 36008392)
122. K. Ahmed, and M.N. Jones The effect of shear on the desorption of liposomes adsorbed to bacterial biofilms J. Liposome Res. 13 2003 187 197 (Pubitemid 36597241)
123. M.L. Immordino, F. Dosio, and L. Cattel Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential Int. J. Nanomed. 1 2006 297 315
124. L. Marcotte, H. Therien-Aubin, C. Sandt, J. Barbeau, and M. Lafleur Solute size effects on the diffusion in biofilms of Streptococcus mutans Biofouling 20 2004 189 201 (Pubitemid 40084532)
125. J.K. Miller, R. Neubig, C.B. Clemons, K.L. Kreider, J.P. Wilber, G.W. Young, A.J. Ditto, Y.H. Yun, A. Milsted, H.T. Badawy, M.J. Panzner, W.J. Youngs, and C.L. Cannon Nanoparticle deposition onto biofilms Ann. Biomed. Eng. 41 2013 53 67
126. M.A. Digman, and E. Gratton Lessons in fluctuation correlation spectroscopy Annu. Rev. Phys. Chem. 62 2011 645 668
127. T.O. Peulen, and K.J. Wilkinson Diffusion of nanoparticles in a biofilm Environ. Sci. Technol. 45 2011 3367 3373
128. O. Habimana, K. Steenkeste, M.P. Fontaine-Aupart, M.N. Bellon-Fontaine, S. Kulakauskas, and R. Briandet Diffusion of nanoparticles in biofilms is altered by bacterial cell wall hydrophobicity Appl. Environ. Microbiol. 77 2010 367 368
129. M.J. Saxton, and K. Jacobson Single-particle tracking: applications to membrane dynamics Annu. Rev. Biophys. Biomol. Struct. 26 1997 373 399 (Pubitemid 27255378)
130. K. Forier, A.S. Messiaen, K. Raemdonck, H. Deschout, J. Rejman, F. De Baets, H. Nelis, S.C. De Smedt, J. Demeester, T. Coenye, and K. Braeckmans Transport of nanoparticles in cystic fibrosis sputum and bacterial biofilms by single-particle tracking microscopy Nanomedicine-UK 8 2013 935 949