Nanoparticles vs. biofilms: a battle against another paradigm of antibiotic resistance

Microbes form surface-adherent community structures called biofilms and these biofilms play a critical role in infection. Biofilms impart antibiotic resistance and sometimes become recalcitrant to the host immune system. It has been reported by the National Institutes of Health that more than 80% of bacterial infections are caused by biofilm formation. Such a kind of infection is also prevalent in biomedical devices which become a source of infection. The treatment of biofilm-mediated infections is a big challenge that requires more sensitive and effective antibiofilm strategies for their removal. Nanoparticles targeting antibiofilm therapy have gained tremendous impetus in the past decade due to their unique features. These nanoparticles are wonder particles having a wide spectrum of biological applications and among these applications their antibiofilm activity is significantly useful. These particles are reactive entities and can easily infiltrate into the matrix which acts as a barrier for many antibiotics. Biomedical surfaces are also nano-functionalized by coating, impregnation or embedding with nanomaterials to prevent biofilm formation. The study of interaction between nanoparticles and biofilms can provide us more insights into the mechanism of biofilm regulation. In this review article, several classes of NPs effective against a broad range of microbial biofilms, both in vivo and in vitro, are described. The application of nanoparticles against biofilms will help to fight resistant infections and will contribute in improving human health.

[1]  Synthesis and characterization of the antibacterial potential of ZnO nanoparticles against extended-spectrum β-lactamases-producing Escherichia coli and Klebsiella pneumoniae isolated from a tertiary care hospital of North India , 2012, Applied Microbiology and Biotechnology.

[2]  B. Kale,et al.  Evaluation of anti-quorum sensing activity of silver nanowires , 2012, Applied Microbiology and Biotechnology.

[3]  Asad U. Khan,et al.  Biofabrication of broad range antibacterial and antibiofilm silver nanoparticles. , 2016, IET nanobiotechnology.

[4]  A. Grumezescu,et al.  Hybrid nanostructured coating for increased resistance of prosthetic devices to staphylococcal colonization , 2013, Nanoscale Research Letters.

[5]  S. Cameotra,et al.  Anti-biofilm efficacy of silver nanoparticles against MRSA and MRSE isolated from wounds in a tertiary care hospital , 2015, Indian journal of medical microbiology.

[6]  T. Wood,et al.  Temporal gene-expression in Escherichia coli K-12 biofilms. , 2007, Environmental microbiology.

[7]  S. Ansari,et al.  Potential applications of enzymes immobilized on/in nano materials: A review. , 2012, Biotechnology advances.

[8]  V. Ramalingam,et al.  Biosynthesis of silver nanoparticles from deep sea bacterium Pseudomonas aeruginosa JQ989348 for antimicrobial, antibiofilm, and cytotoxic activity , 2014, Journal of basic microbiology.

[9]  J. B. Aswathanarayan,et al.  Microbial biofilms and their control by various antimicrobial strategies , 2013 .

[10]  Thomas J Webster,et al.  Antimicrobial applications of nanotechnology: methods and literature , 2012, International journal of nanomedicine.

[11]  S. Dou,et al.  One-pot aqueous synthesis of cysteine-capped CdTe/CdS core–shell nanowires , 2014, Journal of Nanoparticle Research.

[12]  U. Pal,et al.  Effects of crystallization and dopant concentration on the emission behavior of TiO2:Eu nanophosphors , 2012, Nanoscale Research Letters.

[13]  G. O’Toole,et al.  The developmental model of microbial biofilms: ten years of a paradigm up for review. , 2009, Trends in microbiology.

[14]  A. W. Carpenter,et al.  Role of size and shape on biofilm eradication for nitric oxide-releasing silica nanoparticles. , 2013, ACS applied materials & interfaces.

[15]  Asad U. Khan,et al.  International Journal of Nanomedicine , 2022 .

[16]  A. Azam,et al.  Designing and surface modification of zinc oxide nanoparticles for biomedical applications. , 2011, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[17]  J. Barros,et al.  Antibiofilm effects of endodontic sealers containing quaternary ammonium polyethylenimine nanoparticles. , 2014, Journal of endodontics.

[18]  Young Jik Kwon,et al.  "Nanoantibiotics": a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[19]  S. Gangopadhyay,et al.  Ultra-rapid elimination of biofilms via the combustion of a nanoenergetic coating , 2013, BMC Biotechnology.

[20]  M. Chapman,et al.  Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. , 2009, Nature chemical biology.

[21]  Sabine Szunerits,et al.  Inhibition of type 1 fimbriae-mediated Escherichia coli adhesion and biofilm formation by trimeric cluster thiomannosides conjugated to diamond nanoparticles. , 2015, Nanoscale.

[22]  Regine Hengge,et al.  Principles of c-di-GMP signalling in bacteria , 2009, Nature Reviews Microbiology.

[23]  M. Schoenfisch,et al.  Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles. , 2009, Biomaterials.

[24]  A. Gedanken,et al.  A Zn‐Doped CuO Nanocomposite Shows Enhanced Antibiofilm and Antibacterial Activities Against Streptococcus Mutans Compared to Nanosized CuO , 2014 .

[25]  R. Ma,et al.  Use of the quorum sensing inhibitor furanone C-30 to interfere with biofilm formation by Streptococcus mutans and its luxS mutant strain. , 2012, International journal of antimicrobial agents.

[26]  Steven L. Saville,et al.  Discrete nanoparticles induce loss of Legionella pneumophila biofilms from surfaces , 2014, Nanotoxicology.

[27]  D. Grijpma,et al.  Magnetic targeting of surface-modified superparamagnetic iron oxide nanoparticles yields antibacterial efficacy against biofilms of gentamicin-resistant staphylococci. , 2012, Acta biomaterialia.

[28]  K. Neoh,et al.  Nanoparticulates for antibiofilm treatment and effect of aging on its antibacterial activity. , 2010, Journal of endodontics.

[29]  Priya Vashisth,et al.  Rapid efficient synthesis and characterization of silver, gold, and bimetallic nanoparticles from the medicinal plant Plumbago zeylanica and their application in biofilm control , 2014, International journal of nanomedicine.

[30]  P. Stewart,et al.  Role of Antibiotic Penetration Limitation in Klebsiella pneumoniae Biofilm Resistance to Ampicillin and Ciprofloxacin , 2000, Antimicrobial Agents and Chemotherapy.

[31]  S. Chellam,et al.  Synthesis and characterization of lipophilic bismuth dimercaptopropanol nanoparticles and their effects on oral microorganisms growth and biofilm formation , 2014, Journal of Nanoparticle Research.

[32]  D. Mehta,et al.  Bactericidal activity of combinations of Silver-Water Dispersion™ with 19 antibiotics against seven microbial strains , 2006 .

[33]  R. Jayaraman,et al.  Antibiotic resistance: an overview of mechanisms and a paradigm shift , 2009 .

[34]  Aharon Gedanken,et al.  Sonochemical coatings of ZnO and CuO nanoparticles inhibit Streptococcus mutans biofilm formation on teeth model. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[35]  G. James,et al.  Anti-biofilm activity of silver nanoparticles against different microorganisms , 2013, Biofouling.

[36]  Asad U. Khan,et al.  Protein translation machinery holds a key for transition of planktonic cells to biofilm state in Enterococcus faecalis: A proteomic approach. , 2016, Biochemical and biophysical research communications.

[37]  Shaily Mahendra,et al.  Planktonic and biofilm‐grown nitrogen‐cycling bacteria exhibit different susceptibilities to copper nanoparticles , 2015, Environmental toxicology and chemistry.

[38]  P. Dhulster,et al.  Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments , 2014, Archives of Microbiology.

[39]  Jeong Ah Kim,et al.  Inactivation of Pseudomonas aeruginosa PA01 biofilms by hyperthermia using superparamagnetic nanoparticles. , 2011, Journal of microbiological methods.

[40]  Ruchi Yadav,et al.  Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against gram-positive and gram-negative bacteria. , 2010, Nanomedicine : nanotechnology, biology, and medicine.

[41]  A. Gedanken,et al.  Improved antibacterial and antibiofilm activity of magnesium fluoride nanoparticles obtained by water-based ultrasound chemistry. , 2012, Nanomedicine : nanotechnology, biology, and medicine.

[42]  K. Rumbaugh,et al.  The Role of Quorum Sensing in Biofilm Development , 2014 .

[43]  N. Perkas,et al.  ZnO nanoparticle -coated surfaces inhibit bacterial biofilm formation and increase antibiotic susceptibility , 2012 .

[44]  J. Costerton,et al.  Antibody response to Pseudomonas aeruginosa surface protein antigens in a rat model of chronic lung infection. , 1988, Journal of medical microbiology.

[45]  M. Krauze-Baranowska,et al.  Combination of Silver Nanoparticles and Drosera binata Extract as a Possible Alternative for Antibiotic Treatment of Burn Wound Infections Caused by Resistant Staphylococcus aureus , 2014, PloS one.

[46]  A. Kishen,et al.  Role of efflux pump inhibitors on the antibiofilm efficacy of calcium hydroxide, chitosan nanoparticles, and light-activated disinfection. , 2011, Journal of endodontics.

[47]  Aharon Gedanken,et al.  Antibiofilm activity of nanosized magnesium fluoride. , 2009, Biomaterials.

[48]  C. Prestidge,et al.  Liposome-Encapsulated ISMN: A Novel Nitric Oxide-Based Therapeutic Agent against Staphylococcus aureus Biofilms , 2014, PloS one.

[49]  G. Sorial,et al.  Experimental and modeling studies of sorption of ceria nanoparticle on microbial biofilms. , 2014, Bioresource technology.

[50]  J. Costerton,et al.  Bacterial biofilms: a common cause of persistent infections. , 1999, Science.

[51]  Jie Shen,et al.  Lanthanide-doped upconverting luminescent nanoparticle platforms for optical imaging-guided drug delivery and therapy. , 2013, Advanced drug delivery reviews.

[52]  Joshua R. Smith,et al.  Identification of Small Molecules That Antagonize Diguanylate Cyclase Enzymes To Inhibit Biofilm Formation , 2012, Antimicrobial Agents and Chemotherapy.

[53]  W. Verstraete,et al.  Biogenic silver nanoparticles (bio-Ag 0) decrease biofouling of bio-Ag 0/PES nanocomposite membranes. , 2012, Water research.

[54]  Asad U. Khan,et al.  Antibiofilm action of a toluidine blue O-silver nanoparticle conjugate on Streptococcus mutans: a mechanism of type I photodynamic therapy , 2016, Biofouling.

[55]  Michael Y. Galperin,et al.  C‐di‐GMP: the dawning of a novel bacterial signalling system , 2005, Molecular microbiology.

[56]  T. Coenye,et al.  Lipid and polymer nanoparticles for drug delivery to bacterial biofilms. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

[57]  D. Hassett,et al.  Involvement of Nitric Oxide in Biofilm Dispersal of Pseudomonas aeruginosa , 2006, Journal of bacteriology.

[58]  Li-ming Sun,et al.  Characterization, antibiofilm, and mechanism of action of novel PEG-stabilized lipid nanoparticles loaded with terpinen-4-ol. , 2012, Journal of agricultural and food chemistry.

[59]  E. Zubarev,et al.  Therapeutic platforms based on gold nanoparticles and their covalent conjugates with drug molecules. , 2013, Advanced drug delivery reviews.

[60]  M. Lafleur,et al.  Interactions between non-phospholipid liposomes containing cetylpyridinium chloride and biofilms of Streptococcus mutans: modulation of the adhesion and of the biodistribution , 2013, Biofouling.

[61]  D. Freire,et al.  Surfactin reduces the adhesion of food‐borne pathogenic bacteria to solid surfaces , 2009, Letters in applied microbiology.

[62]  I. Chopra,et al.  Increased mutability of Pseudomonas aeruginosa in biofilms. , 2008, The Journal of antimicrobial chemotherapy.

[63]  Asad U. Khan,et al.  Breaking the Spell: Combating Multidrug Resistant ‘Superbugs’ , 2016, Front. Microbiol..

[64]  Ben Wong,et al.  Silver nanoparticles and polymeric medical devices: a new approach to prevention of infection? , 2004, The Journal of antimicrobial chemotherapy.

[65]  A. Gedanken,et al.  Antibiofilm surface functionalization of catheters by magnesium fluoride nanoparticles , 2012, International journal of nanomedicine.

[66]  Milan Kolar,et al.  Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. , 2006, The journal of physical chemistry. B.

[67]  Jie Fu,et al.  Completely "green" synthesis and stabilization of metal nanoparticles. , 2003, Journal of the American Chemical Society.

[68]  K. Chatterjee,et al.  Core/shell nanoparticles in biomedical applications. , 2014, Advances in colloid and interface science.

[69]  W. Tremel,et al.  Vanadium pentoxide nanoparticles mimic vanadium haloperoxidases and thwart biofilm formation. , 2012, Nature nanotechnology.

[70]  M. Doble,et al.  Antibiofilm Properties of Silver and Gold Incorporated PU, PCLm, PC and PMMA Nanocomposites under Two Shear Conditions , 2013, PloS one.

[71]  Xuedong Zhou,et al.  Antibacterial activity and ion release of bonding agent containing amorphous calcium phosphate nanoparticles. , 2014, Dental materials : official publication of the Academy of Dental Materials.

[72]  Philip S. Stewart,et al.  Contributions of Antibiotic Penetration, Oxygen Limitation, and Low Metabolic Activity to Tolerance of Pseudomonas aeruginosa Biofilms to Ciprofloxacin and Tobramycin , 2003, Antimicrobial Agents and Chemotherapy.

[73]  R. Teixeira-Santos,et al.  Polyethyleneimine and polyethyleneimine-based nanoparticles: novel bacterial and yeast biofilm inhibitors. , 2014, Journal of medical microbiology.

[74]  Z. Gong,et al.  Toxicity of silver nanoparticles in zebrafish models , 2008, Nanotechnology.

[75]  R. Hristu,et al.  Hybrid Nanomaterial for Stabilizing the Antibiofilm Activity of Eugenia carryophyllata Essential Oil , 2012, IEEE Transactions on NanoBioscience.

[76]  J. González,et al.  Transport properties of two finite armchair graphene nanoribbons , 2013, Nanoscale Research Letters.

[77]  Sunayana Sitaram,et al.  Antibacterial Efficacy of Iron-Oxide Nanoparticles against Biofilms on Different Biomaterial Surfaces , 2014, International journal of biomaterials.

[78]  J. Friedman,et al.  Amphotericin B releasing nanoparticle topical treatment of Candida spp. in the setting of a burn wound. , 2014, Nanomedicine : nanotechnology, biology, and medicine.

[79]  Xingyu Jiang,et al.  Synergy of non-antibiotic drugs and pyrimidinethiol on gold nanoparticles against superbugs. , 2013, Journal of the American Chemical Society.

[80]  M. Yacamán,et al.  The bactericidal effect of silver nanoparticles , 2005, Nanotechnology.

[81]  J. Costerton,et al.  Prevention and control of bacterial infections associated with medical devices. , 1992, ASAIO journal.

[82]  D. Grainger,et al.  Minimal In Vitro Antimicrobial Efficacy and Ocular Cell Toxicity from Silver Nanoparticles , 2007, Nanobiotechnology : the journal at the intersection of nanotechnology, molecular biology, and biomedical sciences.

[83]  K. Sauer,et al.  The Diguanylate Cyclase GcbA Facilitates Pseudomonas aeruginosa Biofilm Dispersion by Activating BdlA , 2014, Journal of bacteriology.

[84]  Wean Sin Cheow,et al.  The roles of lipid in anti-biofilm efficacy of lipid–polymer hybrid nanoparticles encapsulating antibiotics , 2011 .

[85]  N. Raffaelli,et al.  Monitoring of diguanylate cyclase activity and of cyclic-di-GMP biosynthesis by whole-cell assays suitable for high-throughput screening of biofilm inhibitors , 2009, Applied Microbiology and Biotechnology.

[86]  J. Song,et al.  Does the Antibacterial Activity of Silver Nanoparticles Depend on the Shape of the Nanoparticle? A Study of the Gram-Negative Bacterium Escherichia coli , 2007, Applied and Environmental Microbiology.

[87]  D. Goldmann,et al.  Use of Confocal Microscopy To Analyze the Rate of Vancomycin Penetration through Staphylococcus aureus Biofilms , 2005, Antimicrobial Agents and Chemotherapy.

[88]  Ayusman Sen,et al.  Silver bromide nanoparticle/polymer composites: dual action tunable antimicrobial materials. , 2006, Journal of the American Chemical Society.

[89]  Abraham J Domb,et al.  Surface antimicrobial activity and biocompatibility of incorporated polyethylenimine nanoparticles. , 2008, Biomaterials.

[90]  Yuehe Lin,et al.  Graphene and graphene oxide: biofunctionalization and applications in biotechnology , 2011, Trends in Biotechnology.

[91]  R. Geffers,et al.  SiaA and SiaD are essential for inducing autoaggregation as a specific response to detergent stress in Pseudomonas aeruginosa. , 2009, Environmental microbiology.

[92]  Alexander M Seifalian,et al.  Nanosilver as a new generation of nanoproduct in biomedical applications. , 2010, Trends in biotechnology.

[93]  Roshmi Thomas,et al.  Antibacterial Activity and Synergistic Effect of Biosynthesized AgNPs with Antibiotics Against Multidrug-Resistant Biofilm-Forming Coagulase-Negative Staphylococci Isolated from Clinical Samples , 2014, Applied Biochemistry and Biotechnology.

[94]  T. Webster,et al.  Nanostructured selenium for preventing biofilm formation on polycarbonate medical devices. , 2012, Journal of biomedical materials research. Part A.

[95]  Silver-decorated orthorhombic nanotubes of lithium vanadium oxide: an impeder of bacterial growth and biofilm , 2013, Applied Microbiology and Biotechnology.

[96]  Helmut Münstedt,et al.  Silver ion release from antimicrobial polyamide/silver composites. , 2005, Biomaterials.

[97]  Robert J. Palmer,et al.  Oral multispecies biofilm development and the key role of cell–cell distance , 2010, Nature Reviews Microbiology.

[98]  Non-invasive determination of conjugative transfer of plasmids bearing antibiotic-resistance genes in biofilm-bound bacteria: effects of substrate loading and antibiotic selection , 2012, Applied Microbiology and Biotechnology.

[99]  J. Abraham,et al.  Biosynthesis of Silver Nanoparticles , 2014 .

[100]  Frederick M. Ausubel,et al.  Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation , 2002, Nature.

[101]  P. R. Vuddanda,et al.  Cefuroxime axetil loaded solid lipid nanoparticles for enhanced activity against S. aureus biofilm. , 2014, Colloids and surfaces. B, Biointerfaces.

[102]  Asad U. Khan,et al.  Novel anti-adherence activity of mulberry leaves: inhibition of Streptococcus mutans biofilm by 1-deoxynojirimycin isolated from Morus alba. , 2008, The Journal of antimicrobial chemotherapy.

[103]  H. Nelis,et al.  Transport of Nanoparticles and Tobramycin-loaded Liposomes in Burkholderia cepacia Complex Biofilms , 2013, PloS one.

[104]  R. Donlan Preventing biofilms of clinically relevant organisms using bacteriophage. , 2009, Trends in microbiology.

[105]  F. Protasi,et al.  Potential Antibacterial Activity of Carvacrol-Loaded Poly(DL-lactide-co-glycolide) (PLGA) Nanoparticles against Microbial Biofilm , 2011, International journal of molecular sciences.

[106]  A. Grumezescu,et al.  Hybrid magnetite nanoparticles/Rosmarinus officinalis essential oil nanobiosystem with antibiofilm activity , 2012, Nanoscale Research Letters.

[107]  D. Allison,et al.  Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? , 1988, The Journal of antimicrobial chemotherapy.

[108]  Shakir Khan,et al.  A graphene/zinc oxide nanocomposite film protects dental implant surfaces against cariogenic Streptococcus mutans , 2014, Biofouling.

[109]  F. Fang Antimicrobial reactive oxygen and nitrogen species: concepts and controversies , 2004, Nature Reviews Microbiology.

[110]  Xiang Fei,et al.  Green synthesis of silk fibroin-silver nanoparticle composites with effective antibacterial and biofilm-disrupting properties. , 2013, Biomacromolecules.

[111]  Y. Hwang,et al.  Photoluminescence characteristics of Cd1-xMnxTe single crystals grown by the vertical Bridgman method , 2012, Nanoscale Research Letters.

[112]  S. Cooper,et al.  Bacterial colonization of functionalized polyurethanes. , 2000, Biomaterials.

[113]  Thomas J. Webster,et al.  Reduced Staphylococcus aureus proliferation and biofilm formation on zinc oxide nanoparticle PVC composite surfaces. , 2011, Acta biomaterialia.

[114]  Prof. M.R Shakibaie,et al.  Anti-biofilm activity of biogenic selenium nanoparticles and selenium dioxide against clinical isolates of Staphylococcus aureus, Pseudomonas aeruginosa, and Proteus mirabilis. , 2015, Journal of trace elements in medicine and biology : organ of the Society for Minerals and Trace Elements.

[115]  Mukesh Doble,et al.  Biocompatibility studies on polyaniline and polyaniline-silver nanoparticle coated polyurethane composite. , 2011, Colloids and surfaces. B, Biointerfaces.

[116]  T. Xia,et al.  Understanding biophysicochemical interactions at the nano-bio interface. , 2009, Nature materials.

[117]  David W Williams,et al.  The effect of silver nanoparticles and nystatin on mixed biofilms of Candida glabrata and Candida albicans on acrylic. , 2013, Medical mycology.

[118]  Roberto Kolter,et al.  Biofilms: the matrix revisited. , 2005, Trends in microbiology.

[119]  J. Mattick,et al.  Extracellular DNA required for bacterial biofilm formation. , 2002, Science.

[120]  Biju Jacob,et al.  Toxicity and antibacterial assessment of chitosancoated silver nanoparticles on human pathogens and macrophage cells , 2012, International journal of nanomedicine.

[121]  W. Goessler,et al.  Antibacterial activity of silver and zinc nanoparticles against Vibrio cholerae and enterotoxic Escherichia coli , 2015, International journal of medical microbiology : IJMM.

[122]  J. Maessen,et al.  The relationship between the antimicrobial effect of catheter coatings containing silver nanoparticles and the coagulation of contacting blood. , 2009, Biomaterials.

[123]  N. Høiby,et al.  Phenotypes selected during chronic lung infection in cystic fibrosis patients: implications for the treatment of Pseudomonas aeruginosa biofilm infections. , 2012, FEMS immunology and medical microbiology.

[124]  G. Vinoj,et al.  In Vitro Cytotoxic Effects of Gold Nanoparticles Coated with Functional Acyl Homoserine Lactone Lactonase Protein from Bacillus licheniformis and Their Antibiofilm Activity against Proteus Species , 2014, Antimicrobial Agents and Chemotherapy.

[125]  Lizeng Gao,et al.  Ferromagnetic nanoparticles with peroxidase-like activity enhance the cleavage of biological macromolecules for biofilm elimination. , 2014, Nanoscale.

[126]  L. Visai,et al.  Antibiofilm activity of a monolayer of silver nanoparticles anchored to an amino-silanized glass surface. , 2014, Biomaterials.

[127]  Abraham J Domb,et al.  Polyethyleneimine nanoparticles incorporated into resin composite cause cell death and trigger biofilm stress in vivo , 2010, Proceedings of the National Academy of Sciences.

[128]  D. Fine,et al.  Detachment of Actinobacillus actinomycetemcomitans Biofilm Cells by an Endogenous β-Hexosaminidase Activity , 2003, Journal of bacteriology.

[129]  F. Huang,et al.  The disruption of bacterial membrane integrity through ROS generation induced by nanohybrids of silver and clay. , 2009, Biomaterials.

[130]  Morteza Mahmoudi,et al.  Antibacterial properties of nanoparticles. , 2012, Trends in biotechnology.

[131]  I. Zumeta-Dubé,et al.  Bismuth oxide aqueous colloidal nanoparticles inhibit Candida albicans growth and biofilm formation , 2013, International journal of nanomedicine.

[132]  C. Khursigara,et al.  Synergy of Silver Nanoparticles and Aztreonam against Pseudomonas aeruginosa PAO1 Biofilms , 2014, Antimicrobial Agents and Chemotherapy.

[133]  Ignacio Fuentevilla,et al.  Synthesis of new antibacterial composite coating for titanium based on highly ordered nanoporous silica and silver nanoparticles. , 2014, Materials science & engineering. C, Materials for biological applications.

[134]  S. Kannaiyan,et al.  The Effect of Gold and Iron-Oxide Nanoparticles on Biofilm-Forming Pathogens , 2013, ISRN microbiology.

[135]  R. Hristu,et al.  Inhibitory Activity of ${\rm Fe}_{3} {\rm O}_{4}$/Oleic Acid/Usnic Acid—Core/Shell/Extra-Shell Nanofluid on S. aureus Biofilm Development , 2011, IEEE Transactions on NanoBioscience.

[136]  P. Kanmani,et al.  Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens , 2013 .

[137]  M. Rai,et al.  Silver nanoparticles as a new generation of antimicrobials. , 2009, Biotechnology advances.

[138]  B. Gibbins,et al.  Antimicrobial surface functionalization of plastic catheters by silver nanoparticles. , 2008, The Journal of antimicrobial chemotherapy.

[139]  E. Stobberingh,et al.  The molecular evolution of hospital- and community-associated methicillin-resistant Staphylococcus aureus. , 2009, Current molecular medicine.

[140]  S. Dwivedi,et al.  Reactive Oxygen Species Mediated Bacterial Biofilm Inhibition via Zinc Oxide Nanoparticles and Their Statistical Determination , 2014, PloS one.

[141]  R. Durairaj,et al.  Antibiofilm properties of chemically synthesized silver nanoparticles found against Pseudomonas aeruginosa , 2014, Journal of Nanobiotechnology.

[142]  H. Flemming,et al.  The biofilm matrix , 2010, Nature Reviews Microbiology.

[143]  P. Marcato,et al.  Eco-friendly decoration of graphene oxide with biogenic silver nanoparticles: antibacterial and antibiofilm activity , 2014, Journal of Nanoparticle Research.

[144]  C. Whitchurch,et al.  Non-cytotoxic silver nanoparticle-polyvinyl alcohol hydrogels with anti-biofilm activity: designed as coatings for endotracheal tube materials , 2014, Biofouling.

[145]  R. Losick,et al.  Amyloid fibers provide structural integrity to Bacillus subtilis biofilms , 2010, Proceedings of the National Academy of Sciences.

[146]  L. F. Gorup,et al.  Silver nanoparticles: influence of stabilizing agent and diameter on antifungal activity against Candida albicans and Candida glabrata biofilms , 2012, Letters in applied microbiology.

[147]  L. F. Gorup,et al.  Silver colloidal nanoparticles: antifungal effect against adhered cells and biofilms of Candida albicans and Candida glabrata , 2011, Biofouling.

[148]  Steven J P McInnes,et al.  Nitric oxide-releasing porous silicon nanoparticles , 2014, Nanoscale Research Letters.

[149]  S. Zinjarde,et al.  Psychrotrophic yeast Yarrowia lipolytica NCYC 789 mediates the synthesis of antimicrobial silver nanoparticles via cell-associated melanin , 2013, AMB Express.