Antibiotics Application Strategies to Control Biofilm Formation in Pathogenic Bacteria

Author(s): Fazlurrahman Khan, Dung T.N. Pham, Sandra F. Oloketuyi, Young-Mog Kim*

Journal Name: Current Pharmaceutical Biotechnology

Volume 21 , Issue 4 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Background: The establishment of a biofilm by most pathogenic bacteria has been known as one of the resistance mechanisms against antibiotics. A biofilm is a structural component where the bacterial community adheres to the biotic or abiotic surfaces by the help of Extracellular Polymeric Substances (EPS) produced by bacterial cells. The biofilm matrix possesses the ability to resist several adverse environmental factors, including the effect of antibiotics. Therefore, the resistance of bacterial biofilm-forming cells could be increased up to 1000 times than the planktonic cells, hence requiring a significantly high concentration of antibiotics for treatment.

Methods: Up to the present, several methodologies employing antibiotics as an anti-biofilm, antivirulence or quorum quenching agent have been developed for biofilm inhibition and eradication of a pre-formed mature biofilm.

Results: Among the anti-biofilm strategies being tested, the sub-minimal inhibitory concentration of several antibiotics either alone or in combination has been shown to inhibit biofilm formation and down-regulate the production of virulence factors. The combinatorial strategies include (1) combination of multiple antibiotics, (2) combination of antibiotics with non-antibiotic agents and (3) loading of antibiotics onto a carrier.

Conclusion: The present review paper describes the role of several antibiotics as biofilm inhibitors and also the alternative strategies adopted for applications in eradicating and inhibiting the formation of biofilm by pathogenic bacteria.

Keywords: Antibiotics, biofilm inhibition, virulence factors, resistance mechanism, pathogenic bacteria, multiple antibiotics.

[1]
Fair, R.J.; Tor, Y. Antibiotics and bacterial resistance in the 21st century. Perspect. Medicin. Chem., 2014, 6, 25-64.
[http://dx.doi.org/10.4137/PMC.S14459] [PMID: 25232278]
[2]
Dong, H.; Cao, H.; Zheng, H. Pathogenic bacteria distributions and drug resistance analysis in 96 cases of neonatal sepsis. BMC Pediatr., 2017, 17(1), 44.
[http://dx.doi.org/10.1186/s12887-017-0789-9] [PMID: 28143490]
[3]
Davies, J.; Davies, D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev., 2010, 74(3), 417-433.
[http://dx.doi.org/10.1128/MMBR.00016-10] [PMID: 20805405]
[4]
Li, B.; Webster, T.J. Bacteria antibiotic resistance: New challenges and opportunities for implant-associated orthopedic infections. J. Orthop. Res., 2018, 36(1), 22-32.
[PMID: 28722231]
[5]
van Duin, D.; Paterson, D.L. Multidrug-resistant bacteria in the community: Trends and lessons learned. Infect. Dis. Clin. North Am., 2016, 30(2), 377-390.
[http://dx.doi.org/10.1016/j.idc.2016.02.004] [PMID: 27208764]
[6]
Beceiro, A.; Tomás, M.; Bou, G. Antimicrobial resistance and virulence: a successful or deleterious association in the bacterial world? Clin. Microbiol. Rev., 2013, 26(2), 185-230.
[http://dx.doi.org/10.1128/CMR.00059-12] [PMID: 23554414]
[7]
Martinez, J.L. The role of natural environments in the evolution of resistance traits in pathogenic bacteria. Proc. Biol. Sci., 2009, 276(1667), 2521-2530.
[http://dx.doi.org/10.1098/rspb.2009.0320] [PMID: 19364732]
[8]
Schroeder, M.; Brooks, B.D.; Brooks, A.E. The complex relationship between virulence and antibiotic resistance. Genes (Basel), 2017, 8(1), E39
[http://dx.doi.org/10.3390/genes8010039] [PMID: 28106797]
[9]
Bayramov, D.F.; Neff, J.A. Beyond conventional antibiotics - new directions for combination products to combat biofilm. Adv. Drug Deliv. Rev., 2017, 112, 48-60.
[http://dx.doi.org/10.1016/j.addr.2016.07.010] [PMID: 27496704]
[10]
Ravn, C.; Furustrand Tafin, U.; Bétrisey, B.; Overgaard, S.; Trampuz, A. Reduced ability to detect surface-related biofilm bacteria after antibiotic exposure under in vitro conditions. Acta Orthop., 2016, 87(6), 644-650.
[http://dx.doi.org/10.1080/17453674.2016.1246795] [PMID: 27775462]
[11]
Rendueles, O.; Ghigo, J.M. Multi-species biofilms: How to avoid unfriendly neighbors. FEMS Microbiol. Rev., 2012, 36(5), 972-989.
[http://dx.doi.org/10.1111/j.1574-6976.2012.00328.x] [PMID: 22273363]
[12]
Wiens, J.R.; Vasil, A.I.; Schurr, M.J.; Vasil, M.L. Iron-regulated expression of alginate production, mucoid phenotype, and biofilm formation by Pseudomonas aeruginosa. MBio, 2014, 5(1), e01010-e01013.
[http://dx.doi.org/10.1128/mBio.01010-13] [PMID: 24496793]
[13]
Eze, E.C.; Chenia, H.Y.; El Zowalaty, M.E. Acinetobacter baumannii biofilms: Effects of physicochemical factors, virulence, antibiotic resistance determinants, gene regulation, and future antimicrobial treatments. Infect. Drug Resist., 2018, 11, 2277-2299.
[http://dx.doi.org/10.2147/IDR.S169894] [PMID: 30532562]
[14]
Singh, S.; Singh, S.K.; Chowdhury, I.; Singh, R. Understanding the mechanism of bacterial biofilms resistance to antimicrobial agents. Open Microbiol. J., 2017, 11, 53-62.
[http://dx.doi.org/10.2174/1874285801711010053] [PMID: 28553416]
[15]
Pu, Y.; Zhao, Z.; Li, Y.; Zou, J.; Ma, Q.; Zhao, Y.; Ke, Y.; Zhu, Y.; Chen, H.; Baker, M.A.B.; Ge, H.; Sun, Y.; Xie, X.S.; Bai, F. Enhanced efflux activity facilitates drug tolerance in dormant bacterial cells. Mol. Cell, 2016, 62(2), 284-294.
[http://dx.doi.org/10.1016/j.molcel.2016.03.035] [PMID: 27105118]
[16]
Wood, T.K.; Knabel, S.J.; Kwan, B.W. Bacterial persister cell formation and dormancy. Appl. Environ. Microbiol., 2013, 79(23), 7116-7121.
[http://dx.doi.org/10.1128/AEM.02636-13] [PMID: 24038684]
[17]
Hall, C.W.; Mah, T.F. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol. Rev., 2017, 41(3), 276-301.
[http://dx.doi.org/10.1093/femsre/fux010] [PMID: 28369412]
[18]
Mah, T.F.; O’Toole, G.A. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol., 2001, 9(1), 34-39.
[http://dx.doi.org/10.1016/S0966-842X(00)01913-2] [PMID: 11166241]
[19]
Patel, R. Biofilms and antimicrobial resistance. Clin. Orthop. Relat. Res., 2005, (437), 41-47.
[http://dx.doi.org/10.1097/01.blo.0000175714.68624.74] [PMID: 16056024]
[20]
Pompilio, A.; Crocetta, V.; Savini, V.; Petrelli, D.; Di Nicola, M.; Bucco, S.; Amoroso, L.; Bonomini, M.; Di Bonaventura, G. Phylogenetic relationships, biofilm formation, motility, antibiotic resistance and extended virulence genotypes among Escherichia coli strains from women with community-onset primitive acute pyelonephritis. PLoS One, 2018, 13(5), e0196260
[http://dx.doi.org/10.1371/journal.pone.0196260] [PMID: 29758033]
[21]
Silva, A.J.; Benitez, J.A. Vibrio cholerae biofilms and cholera pathogenesis. PLoS Negl. Trop. Dis., 2016, 10(2), e0004330
[http://dx.doi.org/10.1371/journal.pntd.0004330] [PMID: 26845681]
[22]
Frank, K.L.; Guiton, P.S.; Barnes, A.M.; Manias, D.A.; Chuang-Smith, O.N.; Kohler, P.L.; Spaulding, A.R.; Hultgren, S.J.; Schlievert, P.M.; Dunny, G.M. AhrC and Eep are biofilm infection-associated virulence factors in Enterococcus faecalis. Infect. Immun., 2013, 81(5), 1696-1708.
[http://dx.doi.org/10.1128/IAI.01210-12] [PMID: 23460519]
[23]
Wolcott, R.; Costerton, J.W.; Raoult, D.; Cutler, S.J. The polymicrobial nature of biofilm infection. Clin. Microbiol. Infect., 2013, 19(2), 107-112.
[http://dx.doi.org/10.1111/j.1469-0691.2012.04001.x] [PMID: 22925473]
[24]
Beloin, C.; Renard, S.; Ghigo, J-M.; Lebeaux, D. Novel approaches to combat bacterial biofilms. Curr. Opin. Pharmacol., 2014, 18, 61-68.
[http://dx.doi.org/10.1016/j.coph.2014.09.005] [PMID: 25254624]
[25]
Grassi, L.; Maisetta, G.; Esin, S.; Batoni, G. Combination strategies to enhance the efficacy of antimicrobial peptides against bacterial biofilms. Front. Microbiol., 2017, 8, 2409.
[http://dx.doi.org/10.3389/fmicb.2017.02409] [PMID: 29375486]
[26]
Roy, R.; Tiwari, M.; Donelli, G.; Tiwari, V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence, 2018, 9(1), 522-554.
[http://dx.doi.org/10.1080/21505594.2017.1313372] [PMID: 28362216]
[27]
Subhadra, B.; Kim, D.H.; Woo, K.; Surendran, S.; Choi, C.H. Control of biofilm formation in healthcare: Recent advances exploiting quorum-sensing interference strategies and multidrug efflux pump inhibitors. Materials (Basel), 2018, 11(9), E1676
[http://dx.doi.org/10.3390/ma11091676] [PMID: 30201944]
[28]
Algburi, A.; Comito, N.; Kashtanov, D.; Dicks, L.M.T.; Chikindas, M.L. Control of biofilm formation: Antibiotics and beyond. Appl. Environ. Microbiol., 2017, 83(3), e02508-e02516.
[http://dx.doi.org/10.1128/AEM.02508-16] [PMID: 27864170]
[29]
Oloketuyi, S.F.; Khan, F. Strategies for biofilm inhibition and virulence attenuation of foodborne pathogen-Escherichia coli O157:H7. Curr. Microbiol., 2017, 74(12), 1477-1489.
[http://dx.doi.org/10.1007/s00284-017-1314-y] [PMID: 28744570]
[30]
Oloketuyi, S.F.; Khan, F. Inhibition strategies of Listeria monocytogenes biofilms-current knowledge and future outlooks. J. Basic Microbiol., 2017, 57(9), 728-743.
[http://dx.doi.org/10.1002/jobm.201700071] [PMID: 28594071]
[31]
Khan, F.; Manivasagan, P.; Lee, J-W.; Pham, D.T.N.; Oh, J.; Kim, Y-M. Fucoidan-stabilized gold nanoparticle-mediated biofilm inhibition, attenuation of virulence and motility properties in Pseudomonas aeruginosa PAO1. Mar. Drugs, 2019, 17(4), 208.
[32]
Balaji, K.; Thenmozhi, R.; Pandian, S.K. Effect of subinhibitory concentrations of fluoroquinolones on biofilm production by clinical isolates of Streptococcus pyogenes. Indian J. Med. Res., 2013, 137(5), 963-971.
[PMID: 23760384]
[33]
Aka, S.T.; Haji, S.H. Sub-MIC of antibiotics induced biofilm formation of Pseudomonas aeruginosa in the presence of chlorhexidine. Braz. J. Microbiol., 2015, 46(1), 149-154.
[http://dx.doi.org/10.1590/S1517-838246120140218] [PMID: 26221101]
[34]
Lipp, E.K.; Huq, A.; Colwell, R.R. Effects of global climate on infectious disease: The cholera model. Clin. Microbiol. Rev., 2002, 15(4), 757-770.
[http://dx.doi.org/10.1128/CMR.15.4.757-770.2002] [PMID: 12364378]
[35]
Freire-Moran, L.; Aronsson, B.; Manz, C.; Gyssens, I.C.; So, A.D.; Monnet, D.L.; Cars, O. ECDC-EMA Working Group. Critical shortage of new antibiotics in development against multidrug-resistant bacteria-time to react is now. Drug Resist. Updat., 2011, 14(2), 118-124.
[http://dx.doi.org/10.1016/j.drup.2011.02.003] [PMID: 21435939]
[36]
Van Acker, H.; Van Dijck, P.; Coenye, T. Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol., 2014, 22(6), 326-333.
[http://dx.doi.org/10.1016/j.tim.2014.02.001] [PMID: 24598086]
[37]
Lebeaux, D.; Ghigo, J.M.; Beloin, C. Biofilm-related infections: bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiol. Mol. Biol. Rev., 2014, 78(3), 510-543.
[http://dx.doi.org/10.1128/MMBR.00013-14] [PMID: 25184564]
[38]
Bowler, P.G. Antibiotic resistance and biofilm tolerance: A combined threat in the treatment of chronic infections. J. Wound Care, 2018, 27(5), 273-277.
[http://dx.doi.org/10.12968/jowc.2018.27.5.273] [PMID: 29738295]
[39]
St Denis, T.G.; Dai, T.; Izikson, L.; Astrakas, C.; Anderson, R.R.; Hamblin, M.R.; Tegos, G.P. All you need is light: antimicrobial photoinactivation as an evolving and emerging discovery strategy against infectious disease. Virulence, 2011, 2(6), 509-520.
[http://dx.doi.org/10.4161/viru.2.6.17889] [PMID: 21971183]
[40]
Thomsen, H.; Graf, F.E.; Farewell, A.; Ericson, M.B. Exploring photoinactivation of microbial biofilms using laser scanning microscopy and confined 2-photon excitation. J. Biophotonics, 2018, 11(10), e201800018
[http://dx.doi.org/10.1002/jbio.201800018] [PMID: 29785840]
[41]
de la Fuente-Núñez, C.; Reffuveille, F.; Fernández, L.; Hancock, R.E. Bacterial biofilm development as a multicellular adaptation: Antibiotic resistance and new therapeutic strategies. Curr. Opin. Microbiol., 2013, 16(5), 580-589.
[http://dx.doi.org/10.1016/j.mib.2013.06.013] [PMID: 23880136]
[42]
Maura, D.; Rahme, L.G. Pharmacological inhibition of the Pseudomonas aeruginosa MvfR quorum-sensing system interferes with biofilm formation and potentiates antibiotic-mediated biofilm disruption. Antimicrob. Agents Chemother., 2017, 61(12), e01362-e17.
[http://dx.doi.org/10.1128/AAC.01362-17] [PMID: 28923875]
[43]
Abraham, W.R. Going beyond the control of quorum-sensing to combat biofilm infections. Antibiotics (Basel), 2016, 5(1), E3
[http://dx.doi.org/10.3390/antibiotics5010003] [PMID: 27025518]
[44]
Harms, A.; Maisonneuve, E.; Gerdes, K. Mechanisms of bacterial persistence during stress and antibiotic exposure. Science, 2016, 354(6318)
[http://dx.doi.org/10.1126/science.aaf4268] [PMID: 27980159]
[45]
Gupta, P.; Sarkar, S.; Das, B.; Bhattacharjee, S.; Tribedi, P. Biofilm, pathogenesis and prevention-a journey to break the wall: A review. Arch. Microbiol., 2016, 198(1), 1-15.
[http://dx.doi.org/10.1007/s00203-015-1148-6] [PMID: 26377585]
[46]
Wu, H.; Moser, C.; Wang, H.Z.; Høiby, N.; Song, Z.J. Strategies for combating bacterial biofilm infections. Int. J. Oral Sci., 2015, 7(1), 1-7.
[http://dx.doi.org/10.1038/ijos.2014.65] [PMID: 25504208]
[47]
Tkhilaishvili, T.; Di Luca, M.; Abbandonato, G.; Maiolo, E.M.; Klatt, A.B.; Reuter, M.; Möncke-Buchner, E.; Trampuz, A. Real-time assessment of bacteriophage T3-derived antimicrobial activity against planktonic and biofilm-embedded Escherichia coli by isothermal microcalorimetry. Res. Microbiol., 2018, 169(9), 515-521.
[http://dx.doi.org/10.1016/j.resmic.2018.05.010] [PMID: 29886257]
[48]
Zhang, G.; Liu, J.; Li, R.; Jiao, S.; Feng, C.; Wang, Z.A.; Du, Y. Conjugation of inulin improves anti-biofilm activity of chitosan. Mar. Drugs, 2018, 16(5), E151
[http://dx.doi.org/10.3390/md16050151] [PMID: 29734657]
[49]
Castillo-Juárez, I.; Maeda, T.; Mandujano-Tinoco, E.A.; Tomás, M.; Pérez-Eretza, B.; García-Contreras, S.J.; Wood, T.K.; García-Contreras, R. Role of quorum sensing in bacterial infections. World J. Clin. Cases, 2015, 3(7), 575-598.
[http://dx.doi.org/10.12998/wjcc.v3.i7.575] [PMID: 26244150]
[50]
Antunes, L.C.; Ferreira, R.B.; Buckner, M.M.; Finlay, B.B. Quorum sensing in bacterial virulence. Microbiology, 2010, 156(Pt 8), 2271-2282.
[http://dx.doi.org/10.1099/mic.0.038794-0] [PMID: 20488878]
[51]
Allen, R.C.; Popat, R.; Diggle, S.P.; Brown, S.P. Targeting virulence: Can we make evolution-proof drugs? Nat. Rev. Microbiol., 2014, 12(4), 300-308.
[http://dx.doi.org/10.1038/nrmicro3232] [PMID: 24625893]
[52]
Lee, J.H.; Kim, Y.G.; Lee, K.; Kim, C.J.; Park, D.J.; Ju, Y.; Lee, J.C.; Wood, T.K.; Lee, J. Streptomyces-derived actinomycin D inhibits biofilm formation by Staphylococcus aureus and its hemolytic activity. Biofouling, 2016, 32(1), 45-56.
[http://dx.doi.org/10.1080/08927014.2015.1125888] [PMID: 26785934]
[53]
Saroj, S.D.; Rather, P.N. Streptomycin inhibits quorum sensing in Acinetobacter baumannii. Antimicrob. Agents Chemother., 2013, 57(4), 1926-1929.
[http://dx.doi.org/10.1128/AAC.02161-12] [PMID: 23318804]
[54]
Imperi, F.; Leoni, L.; Visca, P. Antivirulence activity of azithromycin in Pseudomonas aeruginosa. Front. Microbiol., 2014, 5, 178.
[http://dx.doi.org/10.3389/fmicb.2014.00178] [PMID: 24795709]
[55]
Rémy, B.; Mion, S.; Plener, L.; Elias, M.; Chabrière, E.; Daudé, D. Interference in bacterial quorum sensing: A biopharmaceutical perspective. Front. Pharmacol., 2018, 9, 203.
[http://dx.doi.org/10.3389/fphar.2018.00203] [PMID: 29563876]
[56]
Park, J.; Jagasia, R.; Kaufmann, G.F.; Mathison, J.C.; Ruiz, D.I.; Moss, J.A.; Meijler, M.M.; Ulevitch, R.J.; Janda, K.D. Infection control by antibody disruption of bacterial quorum sensing signaling. Chem. Biol., 2007, 14(10), 1119-1127.
[http://dx.doi.org/10.1016/j.chembiol.2007.08.013] [PMID: 17961824]
[57]
LaSarre, B.; Federle, M.J. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol. Mol. Biol. Rev., 2013, 77(1), 73-111.
[http://dx.doi.org/10.1128/MMBR.00046-12] [PMID: 23471618]
[58]
Khan, F.; Javaid, A.; Kim, Y.M. Functional diversity of quorum sensing receptors in pathogenic bacteria: Interspecies, intraspecies and interkingdom level. Curr. Drug Targets, 2019, 20(6), 655-667.
[http://dx.doi.org/10.2174/1389450120666181123123333] [PMID: 30468123]
[59]
Grandclément, C.; Tannières, M.; Moréra, S.; Dessaux, Y.; Faure, D. Quorum quenching: Role in nature and applied developments. FEMS Microbiol. Rev., 2016, 40(1), 86-116.
[http://dx.doi.org/10.1093/femsre/fuv038] [PMID: 26432822]
[60]
Truchado, P.; Giménez-Bastida, J.A.; Larrosa, M.; Castro-Ibáñez, I.; Espín, J.C.; Tomás-Barberán, F.A.; García-Conesa, M.T.; Allende, A. Inhibition of Quorum Sensing (QS) in Yersinia enterocolitica by an orange extract rich in glycosylated flavanones. J. Agric. Food Chem., 2012, 60(36), 8885-8894.
[http://dx.doi.org/10.1021/jf301365a] [PMID: 22533445]
[61]
Lade, H.; Paul, D.; Kweon, J.H. Quorum quenching mediated approaches for control of membrane biofouling. Int. J. Biol. Sci., 2014, 10(5), 550-565.
[http://dx.doi.org/10.7150/ijbs.9028] [PMID: 24910534]
[62]
Uroz, S.; Dessaux, Y.; Oger, P. Quorum sensing and quorum quenching: The yin and yang of bacterial communication. ChemBioChem, 2009, 10(2), 205-216.
[http://dx.doi.org/10.1002/cbic.200800521] [PMID: 19072824]
[63]
Yada, S.; Kamalesh, B.; Sonwane, S.; Guptha, I.; Swetha, R.K. Quorum sensing inhibition, relevance to periodontics. J. Int. Oral Health, 2015, 7(1), 67-69.
[PMID: 25709373]
[64]
Galloway, W.R.; Hodgkinson, J.T.; Bowden, S.; Welch, M.; Spring, D.R. Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends Microbiol., 2012, 20(9), 449-458.
[http://dx.doi.org/10.1016/j.tim.2012.06.003] [PMID: 22771187]
[65]
Walvekar, P.; Gannimani, R.; Govender, T. Combination drug therapy via nanocarriers against infectious diseases. Eur. J. Pharm. Sci., 2019, 127, 121-141.
[http://dx.doi.org/10.1016/j.ejps.2018.10.017] [PMID: 30342173]
[66]
Ghorbani, H.; Memar, M.Y.; Sefidan, F.Y.; Yekani, M.; Ghotaslou, R. In vitro synergy of antibiotic combinations against planktonic and biofilm Pseudomonas aeruginosa. GMS Hyg. Infect. Control, 2017, 12, Doc17.
[PMID: 29094001]
[67]
Komarova, N.L.; Boland, C.R. Cancer: Calculated treatment. Nature, 2013, 499(7458), 291-292.
[http://dx.doi.org/10.1038/499291a] [PMID: 23868257]
[68]
Worthington, R.J.; Melander, C. Combination approaches to combat multidrug-resistant bacteria. Trends Biotechnol., 2013, 31(3), 177-184.
[http://dx.doi.org/10.1016/j.tibtech.2012.12.006] [PMID: 23333434]
[69]
Gill, E.E.; Franco, O.L.; Hancock, R.E. Antibiotic adjuvants: Diverse strategies for controlling drug-resistant pathogens. Chem. Biol. Drug Des., 2015, 85(1), 56-78.
[http://dx.doi.org/10.1111/cbdd.12478] [PMID: 25393203]
[70]
Segev-Zarko, L.; Saar-Dover, R.; Brumfeld, V.; Mangoni, M.L.; Shai, Y. Mechanisms of biofilm inhibition and degradation by antimicrobial peptides. Biochem. J., 2015, 468(2), 259-270.
[http://dx.doi.org/10.1042/BJ20141251] [PMID: 25761937]
[71]
Brooks, B.D.; Brooks, A.E. Therapeutic strategies to combat antibiotic resistance. Adv. Drug Deliv. Rev., 2014, 78, 14-27.
[http://dx.doi.org/10.1016/j.addr.2014.10.027] [PMID: 25450262]
[72]
Tré-Hardy, M.; Nagant, C.; El Manssouri, N.; Vanderbist, F.; Traore, H.; Vaneechoutte, M.; Dehaye, J.P. Efficacy of the combination of tobramycin and a macrolide in an in vitro Pseudomonas aeruginosa mature biofilm model. Antimicrob. Agents Chemother., 2010, 54(10), 4409-4415.
[http://dx.doi.org/10.1128/AAC.00372-10] [PMID: 20696878]
[73]
Gupta, P.; Sarkar, A.; Sandhu, P.; Daware, A.; Das, M.C.; Akhter, Y.; Bhattacharjee, S. Potentiation of antibiotic against Pseudomonas aeruginosa biofilm: A study with plumbagin and gentamicin. J. Appl. Microbiol., 2017, 123(1), 246-261.
[http://dx.doi.org/10.1111/jam.13476] [PMID: 28429871]
[74]
Moon, K.H.; Weber, B.S.; Feldman, M.F. Subinhibitory concentrations of trimethoprim and sulfamethoxazole prevent biofilm formation by Acinetobacter baumannii through inhibition of Csu pilus expression. Antimicrob. Agents Chemother., 2017, 61(9), e00778-e17.
[http://dx.doi.org/10.1128/AAC.00778-17] [PMID: 28674047]
[75]
Elkhatib, W.; Noreddin, A. Efficacy of ciprofloxacin-clarithromycin combination against drug-resistant Pseudomonas aeruginosa mature biofilm using in vitro experimental model. Microb. Drug Resist., 2014, 20(6), 575-582.
[http://dx.doi.org/10.1089/mdr.2014.0024] [PMID: 25050970]
[76]
Fauvart, M.; De Groote, V.N.; Michiels, J. Role of persister cells in chronic infections: Clinical relevance and perspectives on anti-persister therapies. J. Med. Microbiol., 2011, 60(Pt 6), 699-709.
[http://dx.doi.org/10.1099/jmm.0.030932-0] [PMID: 21459912]
[77]
Pamp, S.J.; Gjermansen, M.; Johansen, H.K.; Tolker-Nielsen, T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol. Microbiol., 2008, 68(1), 223-240.
[http://dx.doi.org/10.1111/j.1365-2958.2008.06152.x] [PMID: 18312276]
[78]
Roberts, M.E.; Stewart, P.S. Modelling protection from antimicrobial agents in biofilms through the formation of persister cells. Microbiology, 2005, 151(Pt 1), 75-80.
[http://dx.doi.org/10.1099/mic.0.27385-0] [PMID: 15632427]
[79]
Wright, G.D. Antibiotic adjuvants: Rescuing antibiotics from resistance. Trends Microbiol., 2016, 24(11), 862-871.
[http://dx.doi.org/10.1016/j.tim.2016.06.009] [PMID: 27430191]
[80]
Brackman, G.; Cos, P.; Maes, L.; Nelis, H.J.; Coenye, T. Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob. Agents Chemother., 2011, 55(6), 2655-2661.
[http://dx.doi.org/10.1128/AAC.00045-11] [PMID: 21422204]
[81]
Yang, Y.X.; Xu, Z.H.; Zhang, Y.Q.; Tian, J.; Weng, L.X.; Wang, L.H. A new quorum-sensing inhibitor attenuates virulence and decreases antibiotic resistance in Pseudomonas aeruginosa. J. Microbiol., 2012, 50(6), 987-993.
[http://dx.doi.org/10.1007/s12275-012-2149-7] [PMID: 23274985]
[82]
Fong, J.; Zhang, C.; Yang, R.; Boo, Z.Z.; Tan, S.K.; Nielsen, T.E.; Givskov, M.; Liu, X.W.; Bin, W.; Su, H.; Yang, L. Combination therapy strategy of quorum quenching enzyme and quorum sensing inhibitor in suppressing multiple quorum sensing pathways of P. aeruginosa. Sci. Rep., 2018, 8(1), 1155.
[http://dx.doi.org/10.1038/s41598-018-19504-w] [PMID: 29348452]
[83]
Wang, H.; Gill, C.J.; Lee, S.H.; Mann, P.; Zuck, P.; Meredith, T.C.; Murgolo, N.; She, X.; Kales, S.; Liang, L.; Liu, J.; Wu, J.; Santa Maria, J.; Su, J.; Pan, J.; Hailey, J.; Mcguinness, D.; Tan, C.M.; Flattery, A.; Walker, S.; Black, T.; Roemer, T. Discovery of wall teichoic acid inhibitors as potential anti-MRSA β-lactam combination agents. Chem. Biol., 2013, 20(2), 272-284.
[http://dx.doi.org/10.1016/j.chembiol.2012.11.013] [PMID: 23438756]
[84]
Antonoplis, A.; Zang, X.; Huttner, M.A.; Chong, K.K.L.; Lee, Y.B.; Co, J.Y.; Amieva, M.R.; Kline, K.A.; Wender, P.A.; Cegelski, L. A Dual-function antibiotic-transporter conjugate exhibits superior activity in sterilizing MRSA biofilms and killing persister cells. J. Am. Chem. Soc., 2018, 140(47), 16140-16151.
[http://dx.doi.org/10.1021/jacs.8b08711] [PMID: 30388366]
[85]
Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415(6870), 389-395.
[http://dx.doi.org/10.1038/415389a] [PMID: 11807545]
[86]
Hollmann, A.; Martinez, M.; Maturana, P.; Semorile, L.C.; Maffia, P.C. Antimicrobial peptides: Interaction with model and biological membranes and synergism with chemical antibiotics. Front Chem., 2018, 6, 204.
[http://dx.doi.org/10.3389/fchem.2018.00204] [PMID: 29922648]
[87]
Jorge, P.; Lourenço, A.; Pereira, M.O. New trends in peptide-based anti-biofilm strategies: A review of recent achievements and bioinformatic approaches. Biofouling, 2012, 28(10), 1033-1061.
[http://dx.doi.org/10.1080/08927014.2012.728210] [PMID: 23016989]
[88]
Park, S.C.; Park, Y.; Hahm, K.S. The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. Int. J. Mol. Sci., 2011, 12(9), 5971-5992.
[http://dx.doi.org/10.3390/ijms12095971] [PMID: 22016639]
[89]
Di Luca, M.; Maccari, G.; Nifosì, R. Treatment of microbial biofilms in the post-antibiotic era: Prophylactic and therapeutic use of antimicrobial peptides and their design by bioinformatics tools. Pathog. Dis., 2014, 70(3), 257-270.
[http://dx.doi.org/10.1111/2049-632X.12151] [PMID: 24515391]
[90]
Chung, P.Y.; Khanum, R. Antimicrobial peptides as potential anti-biofilm agents against multidrug-resistant bacteria. J. Microbiol. Immunol. Infect., 2017, 50(4), 405-410.
[http://dx.doi.org/10.1016/j.jmii.2016.12.005] [PMID: 28690026]
[91]
Dosler, S.; Karaaslan, E.; Alev Gerceker, A. Antibacterial and anti-biofilm activities of melittin and colistin, alone and in combination with antibiotics against Gram-negative bacteria. J. Chemother., 2016, 28(2), 95-103.
[http://dx.doi.org/10.1179/1973947815Y.0000000004] [PMID: 25801062]
[92]
Mataraci, E.; Dosler, S. In vitro activities of antibiotics and antimicrobial cationic peptides alone and in combination against methicillin-resistant Staphylococcus aureus biofilms. Antimicrob. Agents Chemother., 2012, 56(12), 6366-6371.
[http://dx.doi.org/10.1128/AAC.01180-12] [PMID: 23070152]
[93]
Heinbockel, L.; Weindl, G.; Martinez-de-Tejada, G.; Correa, W.; Sanchez-Gomez, S.; Bárcena-Varela, S.; Goldmann, T.; Garidel, P.; Gutsmann, T.; Brandenburg, K. Inhibition of lipopolysaccharide- and lipoprotein-induced inflammation by antitoxin peptide Pep19-2.5. Front. Immunol., 2018, 9, 1704.
[http://dx.doi.org/10.3389/fimmu.2018.01704] [PMID: 30093904]
[94]
Bessa, L.J.; Eaton, P.; Dematei, A.; Plácido, A.; Vale, N.; Gomes, P.; Delerue-Matos, C.; Sa Leite, J.R.; Gameiro, P. Synergistic and antibiofilm properties of ocellatin peptides against multidrug-resistant Pseudomonas aeruginosa. Future Microbiol., 2018, 13, 151-163.
[http://dx.doi.org/10.2217/fmb-2017-0175] [PMID: 29308671]
[95]
Hu, C.M.; Aryal, S.; Zhang, L. Nanoparticle-assisted combination therapies for effective cancer treatment. Ther. Deliv., 2010, 1(2), 323-334.
[http://dx.doi.org/10.4155/tde.10.13] [PMID: 22816135]
[96]
Wang, L.; Hu, C.; Shao, L. The antimicrobial activity of nanoparticles: Present situation and prospects for the future. Int. J. Nanomedicine, 2017, 12, 1227-1249.
[http://dx.doi.org/10.2147/IJN.S121956] [PMID: 28243086]
[97]
Jiang, L.; Lin, J.; Taggart, C.C.; Bengoechea, J.A.; Scott, C.J. Nanodelivery strategies for the treatment of multidrug-resistant bacterial infections. J. Interdiscip. Nanomed., 2018, 3(3), 111-121.
[http://dx.doi.org/10.1002/jin2.48] [PMID: 30443410]
[98]
Forier, K.; Raemdonck, K.; De Smedt, S.C.; Demeester, J.; Coenye, T.; Braeckmans, K. Lipid and polymer nanoparticles for drug delivery to bacterial biofilms. J. Control. Release, 2014, 190, 607-623.
[http://dx.doi.org/10.1016/j.jconrel.2014.03.055] [PMID: 24794896]
[99]
Drulis-Kawa, Z.; Dorotkiewicz-Jach, A. Liposomes as delivery systems for antibiotics. Int. J. Pharm., 2010, 387(1-2), 187-198.
[http://dx.doi.org/10.1016/j.ijpharm.2009.11.033] [PMID: 19969054]
[100]
Jamil, B.; Habib, H.; Abbasi, S.A.; Ihsan, A.; Nasir, H.; Imran, M. Development of cefotaxime impregnated chitosan as nano-antibiotics: De novo strategy to combat biofilm forming multi-drug resistant pathogens. Front. Microbiol., 2016, 7, 330.
[http://dx.doi.org/10.3389/fmicb.2016.00330] [PMID: 27047457]
[101]
Hwang, I.S.; Hwang, J.H.; Choi, H.; Kim, K.J.; Lee, D.G. Synergistic effects between silver nanoparticles and antibiotics and the mechanisms involved. J. Med. Microbiol., 2012, 61(Pt 12), 1719-1726.
[http://dx.doi.org/10.1099/jmm.0.047100-0] [PMID: 22956753]
[102]
Zhang, X.; Zhang, W.; Liu, L.; Yang, M.; Huang, L.; Chen, K.; Wang, R.; Yang, B.; Zhang, D.; Wang, J. Antibiotic-loaded MoS2 nanosheets to combat bacterial resistance via biofilm inhibition. Nanotechnology, 2017, 28(22), 225101
[http://dx.doi.org/10.1088/1361-6528/aa6c9b] [PMID: 28480869]
[103]
Smith, A.W. Biofilms and antibiotic therapy: Is there a role for combating bacterial resistance by the use of novel drug delivery systems? Adv. Drug Deliv. Rev., 2005, 57(10), 1539-1550.
[http://dx.doi.org/10.1016/j.addr.2005.04.007] [PMID: 15950314]
[104]
Campoccia, D.; Montanaro, L.; Speziale, P.; Arciola, C.R. Antibiotic-loaded biomaterials and the risks for the spread of antibiotic resistance following their prophylactic and therapeutic clinical use. Biomaterials, 2010, 31(25), 6363-6377.
[http://dx.doi.org/10.1016/j.biomaterials.2010.05.005] [PMID: 20542556]
[105]
Khan, F.; Khan, M.M.; Kim, Y.M. Recent progress and future perspectives of antibiofilm drugs immobilized on nanomaterials. Curr. Pharm. Biotechnol., 2018, 19(8), 631-643.
[http://dx.doi.org/10.2174/1389201019666180828090052] [PMID: 30152281]
[106]
Xie, S.; Tao, Y.; Pan, Y.; Qu, W.; Cheng, G.; Huang, L.; Chen, D.; Wang, X.; Liu, Z.; Yuan, Z. Biodegradable nanoparticles for intracellular delivery of antimicrobial agents. J. Control. Release, 2014, 187, 101-117.
[http://dx.doi.org/10.1016/j.jconrel.2014.05.034] [PMID: 24878179]
[107]
Alhariri, M.; Majrashi, M.A.; Bahkali, A.H.; Almajed, F.S.; Azghani, A.O.; Khiyami, M.A.; Alyamani, E.J.; Aljohani, S.M.; Halwani, M.A. Efficacy of neutral and negatively charged liposome-loaded gentamicin on planktonic bacteria and biofilm communities. Int. J. Nanomedicine, 2017, 12, 6949-6961.
[http://dx.doi.org/10.2147/IJN.S141709] [PMID: 29075113]
[108]
Habash, M.B.; Goodyear, M.C.; Park, A.J.; Surette, M.D.; Vis, E.C.; Harris, R.J.; Khursigara, C.M. Potentiation of tobramycin by silver nanoparticles against Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother., 2017, 61(11), e00415-e00417.
[http://dx.doi.org/10.1128/AAC.00415-17] [PMID: 28848007]
[109]
Hadinoto, K.; Cheow, W.S. Nano-antibiotics in chronic lung infection therapy against Pseudomonas aeruginosa. Colloids Surf. B Biointerfaces, 2014, 116, 772-785.
[http://dx.doi.org/10.1016/j.colsurfb.2014.02.032] [PMID: 24656614]
[110]
Rukavina, Z.; Šegvić Klarić, M.; 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.
[http://dx.doi.org/10.1016/j.ijpharm.2018.10.024] [PMID: 30312749]
[111]
Andrade, F.; Rafael, D.; Videira, M.; Ferreira, D.; Sosnik, A.; Sarmento, B. Nanotechnology and pulmonary delivery to overcome resistance in infectious diseases. Adv. Drug Deliv. Rev., 2013, 65(13-14), 1816-1827.
[http://dx.doi.org/10.1016/j.addr.2013.07.020] [PMID: 23932923]
[112]
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.
[http://dx.doi.org/10.1128/AAC.00235-13] [PMID: 23545534]
[113]
Gupta, P.V.; Nirwane, A.M.; Belubbi, T.; Nagarsenker, M.S. Pulmonary delivery of synergistic combination of fluoroquinolone antibiotic complemented with proteolytic enzyme: A novel antimicrobial and antibiofilm strategy. Nanomedicine (Lond.), 2017, 13(7), 2371-2384.
[http://dx.doi.org/10.1016/j.nano.2017.06.011] [PMID: 28648640]
[114]
Ye, T.; Sun, S.; Sugianto, T.D.; Tang, P.; Parumasivam, T.; Chang, Y.K.; Astudillo, A.; Wang, S.; Chan, H.K. Novel combination proliposomes containing tobramycin and clarithromycin effective against Pseudomonas aeruginosa biofilms. Int. J. Pharm., 2018, 552(1-2), 130-138.
[http://dx.doi.org/10.1016/j.ijpharm.2018.09.061] [PMID: 30267753]
[115]
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
[http://dx.doi.org/10.1371/journal.pone.0079220] [PMID: 24244452]
[116]
Javaid, A.; Oloketuyi, S.F.; Khan, M.M.; Khan, F. Diversity of bacterial synthesis of silver nanoparticles. Bionanoscience, 2018, 8(1), 43-59.
[117]
Wells, C.M.; Beenken, K.E.; Smeltzer, M.S.; Courtney, H.S.; Jennings, J.A.; Haggard, W.O. Ciprofloxacin and rifampin dual antibiotic-loaded biopolymer chitosan sponge for bacterial inhibition. Mil. Med., 2018, 183(Suppl. 1), 433-444.
[http://dx.doi.org/10.1093/milmed/usx150]
[118]
Baelo, A.; Levato, R.; Julián, E.; Crespo, A.; Astola, J.; Gavaldà, J.; Engel, E.; Mateos-Timoneda, M.A.; Torrents, E. Disassembling bacterial extracellular matrix with DNase-coated nanoparticles to enhance antibiotic delivery in biofilm infections. J. Control. Release, 2015, 209, 150-158.
[http://dx.doi.org/10.1016/j.jconrel.2015.04.028] [PMID: 25913364]
[119]
Ashbaugh, A.G.; Jiang, X.; Zheng, J.; Tsai, A.S.; Kim, W.S.; Thompson, J.M.; Miller, R.J.; Shahbazian, J.H.; Wang, Y.; Dillen, C.A.; Ordonez, A.A.; Chang, Y.S.; Jain, S.K.; Jones, L.C.; Sterling, R.S.; Mao, H.Q.; Miller, L.S. Polymeric nanofiber coating with tunable combinatorial antibiotic delivery prevents biofilm-associated infection in vivo. Proc. Natl. Acad. Sci. USA, 2016, 113(45), E6919-E6928.
[http://dx.doi.org/10.1073/pnas.1613722113] [PMID: 27791154]
[120]
Shrestha, A.; Hamblin, M.R.; Kishen, A. Characterization of a conjugate between Rose Bengal and chitosan for targeted antibiofilm and tissue stabilization effects as a potential treatment of infected dentin. Antimicrob. Agents Chemother., 2012, 56(9), 4876-4884.
[http://dx.doi.org/10.1128/AAC.00810-12] [PMID: 22777042]
[121]
Goy, R.C.; Britto, D.D.; Assis, O.B.G. A review of the antimicrobial activity of chitosan. Polímeros, 2009, 19, 241-247.
[122]
Khan, F.; Manivasagan, P.; Pham, D.T.N.; Oh, J.; Kim, S.K.; Kim, Y.M. Antibiofilm and antivirulence properties of chitosan-polypyrrole nanocomposites to Pseudomonas aeruginosa. Microb. Pathog., 2019, 128, 363-373.
[http://dx.doi.org/10.1016/j.micpath.2019.01.033] [PMID: 30684638]
[123]
Zhu, X.; Liu, D.; Singh, A.K.; Drolia, R.; Bai, X.; Tenguria, S.; Bhunia, A.K. Tunicamycin mediated inhibition of wall teichoic acid affects Staphylococcus aureus and Listeria monocytogenes cell morphology, biofilm formation and virulence. Front. Microbiol., 2018, 9, 1352.
[http://dx.doi.org/10.3389/fmicb.2018.01352] [PMID: 30034372]
[124]
Ding, W.; Zhou, Y.; Qu, Q.; Cui, W. God’s power, B.O.; Liu, Y.; Chen, X.; Chen, M.; Yang, Y.; Li, Y. Azithromycin inhibits biofilm formation by Staphylococcus xylosus and affects histidine biosynthesis pathway. Front. Pharmacol., 2018, 9, 740.
[http://dx.doi.org/10.3389/fphar.2018.00740] [PMID: 30042679]
[125]
Carbone, A.; Parrino, B.; Cusimano, M.G.; Spanò, V.; Montalbano, A.; Barraja, P.; Schillaci, D.; Cirrincione, G.; Diana, P.; Cascioferro, S. New thiazole nortopsentin analogues inhibit bacterial biofilm formation. Mar. Drugs, 2018, 16(8), E274
[http://dx.doi.org/10.3390/md16080274] [PMID: 30081568]
[126]
Singh, S.; Bhatia, S. In silico identification of albendazole as a quorum sensing inhibitor and its in vitro verification using CviR and LasB receptors based assay systems. Bioimpacts, 2018, 8(3), 201-209.
[http://dx.doi.org/10.15171/bi.2018.23] [PMID: 30211080]
[127]
Anderson, G.G.; Kenney, T.F.; Macleod, D.L.; Henig, N.R.; O’Toole, G.A. Eradication of Pseudomonas aeruginosa biofilms on cultured airway cells by a fosfomycin/tobramycin antibiotic combination. Pathog. Dis., 2013, 67(1), 39-45.
[http://dx.doi.org/10.1111/2049-632X.12015] [PMID: 23620118]
[128]
Thellin, O.; Zorzi, W.; Jolois, O.; Elmoualij, B.; Duysens, G.; Cahay, B.; Streel, B.; Charif, M.; Bastin, R.; Heinen, E.; Quatresooz, P. In vitro approach to study the synergistic effects of tobramycin and clarithromycin against Pseudomonas aeruginosa biofilms using prokaryotic or eukaryotic culture media. Int. J. Antimicrob. Agents, 2015, 46(1), 33-38.
[http://dx.doi.org/10.1016/j.ijantimicag.2015.02.010] [PMID: 25963337]
[129]
Wang, A.; Wang, Q.; Kudinha, T.; Xiao, S.; Zhuo, C. Effects of fluoroquinolones and azithromycin on biofilm formation of Stenotrophomonas maltophilia. Sci. Rep., 2016, 6, 29701.
[http://dx.doi.org/10.1038/srep29701] [PMID: 27405358]
[130]
Tezel, B.U.; Akçelik, N.; Yüksel, F.N.; Karatuğ, N.T.; Akçelik, M. Effects of sub-MIC antibiotic concentrations on biofilm production of Salmonella Infan. Biotechnol. Biotechnol. Equip., 2016, 30(6), 1184-1191.
[http://dx.doi.org/10.1080/13102818.2016.1224981]
[131]
Anderl, J.N.; Franklin, M.J.; Stewart, P.S. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother., 2000, 44(7), 1818-1824.
[http://dx.doi.org/10.1128/AAC.44.7.1818-1824.2000] [PMID: 10858336]
[132]
Raad, I.; Darouiche, R.; Hachem, R.; Sacilowski, M.; Bodey, G.P. Antibiotics and prevention of microbial colonization of catheters. Antimicrob. Agents Chemother., 1995, 39(11), 2397-2400.
[http://dx.doi.org/10.1128/AAC.39.11.2397] [PMID: 8585715]
[133]
Henry-Stanley, M.J.; Hess, D.J.; Wells, C.L. Aminoglycoside inhibition of Staphylococcus aureus biofilm formation is nutrient dependent. J. Med. Microbiol., 2014, 63(Pt 6), 861-869.
[http://dx.doi.org/10.1099/jmm.0.068130-0] [PMID: 24696518]
[134]
Majidpour, A.; Fathizadeh, S.; Afshar, M.; Rahbar, M.; Boustanshenas, M.; Heidarzadeh, M.; Arbabi, L.; Soleymanzadeh Moghadam, S. Dose-dependent effects of common antibiotics used to treat Staphylococcus aureus on biofilm formation. Iran. J. Pathol., 2017, 12(4), 362-370.
[PMID: 29563932]
[135]
She, P.; Luo, Z.; Chen, L.; Wu, Y. Efficacy of levofloxacin against biofilms of Pseudomonas aeruginosa isolated from patients with respiratory tract infections in vitro. MicrobiologyOpen, 2019, 8(5), e00720
[http://dx.doi.org/10.1002/mbo3.720] [PMID: 30183143]
[136]
Karczewski, A.; Feitosa, S.A.; Hamer, E.I.; Pankajakshan, D.; Gregory, R.L.; Spolnik, K.J.; Bottino, M.C. Clindamycin-modified triple antibiotic nanofibers: A stain-free antimicrobial intracanal drug delivery system. J. Endod., 2018, 44(1), 155-162.
[http://dx.doi.org/10.1016/j.joen.2017.08.024] [PMID: 29061356]
[137]
Bardbari, A.M.; Arabestani, M.R.; Karami, M.; Keramat, F.; Aghazadeh, H.; Alikhani, M.Y.; Bagheri, K.P. Highly synergistic activity of melittin with imipenem and colistin in biofilm inhibition against multidrug-resistant strong biofilm producer strains of Acinetobacter baumannii. Eur. J. Clin. Microbiol. Infect. Dis., 2018, 37(3), 443-454.
[http://dx.doi.org/10.1007/s10096-018-3189-7] [PMID: 29353377]
[138]
Wunnoo, S.; Saising, J.; Voravuthikunchai, S.P. Rhodomyrtone inhibits lipase production, biofilm formation, and disorganizes established biofilm in Propionibacterium acnes. Anaerobe, 2017, 43, 61-68.
[http://dx.doi.org/10.1016/j.anaerobe.2016.12.002] [PMID: 27923605]
[139]
Tan, L.Z.W.; Hong, Z.; Yam, J.K.H.; Salido, M.M.S.; Woo, B.Y.; Li, S.F.Y.; Yang, L.; Givskov, M.; Chng, S-S. Auranofin inhibits virulence in Pseudomonas aeruginosa. bioRxiv, 2017., 198820
[http://dx.doi.org/10.1101/198820]
[140]
Yuyama, K.T.; Neves, T.S.P.D.C.; Memória, M.T.; Tartuci, I.T.; Abraham, W-R. Aurantiogliocladin inhibits biofilm formation at subtoxic concentrations. AIMS Microbiol, 2017, 3(1), 50-60.
[http://dx.doi.org/10.3934/microbiol.2017.1.50] [PMID: 31294148]
[141]
Ong, H.S.; Oettinger-Barak, O.; Dashper, S.G.; Darby, I.B.; Tan, K.H.; Reynolds, E.C. Effect of azithromycin on a red complex polymicrobial biofilm. J. Oral Microbiol., 2017, 9(1), 1339579
[http://dx.doi.org/10.1080/20002297.2017.1339579] [PMID: 28748041]
[142]
Mohamed, S.H.; Mohamed, M.S.M.; Khalil, M.S.; Azmy, M.; Mabrouk, M.I. Combination of essential oil and ciprofloxacin to inhibit/eradicate biofilms in multidrug-resistant Klebsiella pneumoniae. J. Appl. Microbiol., 2018, 125(1), 84-95.
[http://dx.doi.org/10.1111/jam.13755] [PMID: 29517825]
[143]
Zhang, A.; Mu, H.; Zhang, W.; Cui, G.; Zhu, J.; Duan, J. Chitosan coupling makes microbial biofilms susceptible to antibiotics. Sci. Rep., 2013, 3, 3364.
[http://dx.doi.org/10.1038/srep03364] [PMID: 24284335]
[144]
She, P.; Wang, Y.; Luo, Z.; Chen, L.; Tan, R.; Wang, Y.; Wu, Y. Meloxicam inhibits biofilm formation and enhances antimicrobial agents efficacy by Pseudomonas aeruginosa. Microbiol.Open, 2018, 7(1)
[http://dx.doi.org/10.1002/mbo3.545] [PMID: 29178590]
[145]
Belfield, K.; Bayston, R.; Hajduk, N.; Levell, G.; Birchall, J.P.; Daniel, M. Evaluation of combinations of putative anti-biofilm agents and antibiotics to eradicate biofilms of Staphylococcus aureus and Pseudomonas aeruginosa. J. Antimicrob. Chemother., 2017, 72(9), 2531-2538.
[http://dx.doi.org/10.1093/jac/dkx192] [PMID: 28859444]
[146]
Maiden, M.M.; Hunt, A.M.A.; Zachos, M.P.; Gibson, J.A.; Hurwitz, M.E.; Mulks, M.H.; Waters, C.M. Triclosan is an aminoglycoside adjuvant for eradication of Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother., 2018, 62(6), e00146-e18.
[http://dx.doi.org/10.1128/AAC.00146-18] [PMID: 29661867]
[147]
Dosler, S.; Mataraci, E. In vitro pharmacokinetics of antimicrobial cationic peptides alone and in combination with antibiotics against methicillin resistant Staphylococcus aureus biofilms. Peptides, 2013, 49, 53-58.
[http://dx.doi.org/10.1016/j.peptides.2013.08.008] [PMID: 23988790]
[148]
Xu, N.; Cheng, H.; Xu, J.; Li, F.; Gao, B.; Li, Z.; Gao, C.; Huo, K.; Fu, J.; Xiong, W. Silver-loaded nanotubular structures enhanced bactericidal efficiency of antibiotics with synergistic effect in vitro and in vivo. Int. J. Nanomedicine, 2017, 12, 731-743.
[http://dx.doi.org/10.2147/IJN.S123648] [PMID: 28184157]
[149]
Nair, S.; Desai, S.; Poonacha, N.; Vipra, A.; Sharma, U. Antibiofilm activity and synergistic inhibition of Staphylococcus aureus biofilms by bactericidal protein P128 in combination with antibiotics. Antimicrob. Agents Chemother., 2016, 60(12), 7280-7289.
[PMID: 27671070]
[150]
Breser, M.L.; Felipe, V.; Bohl, L.P.; Orellano, M.S.; Isaac, P.; Conesa, A.; Rivero, V.E.; Correa, S.G.; Bianco, I.D.; Porporatto, C. Chitosan and cloxacillin combination improve antibiotic efficacy against different lifestyle of coagulase-negative Staphylococcus isolates from chronic bovine mastitis. Sci. Rep., 2018, 8(1), 5081.
[http://dx.doi.org/10.1038/s41598-018-23521-0] [PMID: 29572457]
[151]
Hou, Y.; Wang, Z.; Zhang, P.; Bai, H.; Sun, Y.; Duan, J.; Mu, H. Lysozyme associated liposomal gentamicin inhibits bacterial biofilm. Int. J. Mol. Sci., 2017, 18(4), E784
[http://dx.doi.org/10.3390/ijms18040784] [PMID: 28397768]
[152]
Paganelli, F.L.; van de Kamer, T.; Brouwer, E.C.; Leavis, H.L.; Woodford, N.; Bonten, M.J.; Willems, R.J.; Hendrickx, A.P. Lipoteichoic acid synthesis inhibition in combination with antibiotics abrogates growth of multidrug-resistant Enterococcus faecium. Int. J. Antimicrob. Agents, 2017, 49(3), 355-363.
[http://dx.doi.org/10.1016/j.ijantimicag.2016.12.002] [PMID: 28188831]
[153]
Duan, F.; Feng, X.; Jin, Y.; Liu, D.; Yang, X.; Zhou, G.; Liu, D.; Li, Z.; Liang, X.J.; Zhang, J. Metal-carbenicillin framework-based nanoantibiotics with enhanced penetration and highly efficient inhibition of MRSA. Biomaterials, 2017, 144, 155-165.
[http://dx.doi.org/10.1016/j.biomaterials.2017.08.024] [PMID: 28834764]
[154]
Mala, R.; Annie Aglin, A.; Ruby Celsia, A.S.; Geerthika, S.; Kiruthika, N.; Vazaga, P.C.; Srinivasa, K.K. Foley catheters functionalised with a synergistic combination of antibiotics and silver nanoparticles resist biofilm formation. IET Nanobiotechnol., 2017, 11(5), 612-620.
[http://dx.doi.org/10.1049/iet-nbt.2016.0148] [PMID: 28745297]
[155]
Garbacz, K.; Kamysz, W.; Piechowicz, L. Activity of antimicrobial peptides, alone or combined with conventional antibiotics, against Staphylococcus aureus isolated from the airways of cystic fibrosis patients. Virulence, 2017, 8(1), 94-100.
[http://dx.doi.org/10.1080/21505594.2016.1213475] [PMID: 27450039]
[156]
Lijuan, C.; Xing, Y.; Minxi, W.; Wenkai, L.; Le, D. Development of an aptamer-ampicillin conjugate for treating biofilms. Biochem. Biophys. Res. Commun., 2017, 483(2), 847-854.
[http://dx.doi.org/10.1016/j.bbrc.2017.01.016] [PMID: 28069377]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 4
Year: 2020
Published on: 25 March, 2020
Page: [270 - 286]
Pages: 17
DOI: 10.2174/1389201020666191112155905
Price: $65

Article Metrics

PDF: 33
HTML: 9
EPUB: 1
PRC: 1