Abstract
The emergence of multidrug-resistant (MDR) pathogens is a major problem in the therapeutic management of infectious diseases. Among the bacterial resistance mechanisms is the development of an enveloped protein and polysaccharide-hydrated matrix called a biofilm. Polyphenolics have demonstrated beneficial antibacterial effects. Phenolic compounds mediate their antibiofilm effects via disruption of the bacterial membrane, deprivation of substrate, protein binding, binding to adhesion complex, viral fusion blockage and interactions with eukaryotic DNA. However, these compounds have limitations of chemical instability, low bioavailability, poor water solubility and short half-lives. Nanoformulations offer a promising solution to overcome these challenges by enhancing their antibacterial potential. This review summarizes the antibiofilm role of polyphenolics, their underlying mechanisms and their potential role as resistance-modifying agents.
Plain language summary
Bacteria can become more difficult to kill by forming a protective layer called a biofilm. This is a problem because infections caused by these bacteria can be difficult to treat. Polyphenols are a natural compound found in plants. They have shown promise in fighting resistant bacteria by stopping bacteria from forming a biofilm. However, polyphenols have some limitations. These limitations can be overcome by using nanomaterials, which are types of tiny particles. When polyphenols are combined with nanomaterials, they become much better at fighting bacteria. This is a promising solution to treating resistant infections caused by biofilm-forming bacteria.
Tweetable abstract
Polyphenols combat bacterial biofilm, a major resistance factor, via multiple mechanisms. Nanoformulations could boost their antibacterial power.
Papers of special note have been highlighted as: • of interest; •• of considerable interest
References
- 1. . Nanoantibiotics: recent developments and future prospects. Front. Clin. Drug Res. Anti. Infect. 5, 158–182 (2019). •• Authors presentthe concept of nano-antibiotics. Compared with conventional antibiotics, they are a safe and effective alternative approach with better pharmacokinetics and dynamics profiles.
- 2. . Antibiotics: past, present and future. Curr. Opin. Microbiol. 51, 72–80 (2019).
- 3. . WHO European strategic action plan on antibiotic resistance: how to preserve antibiotics. J. Pediatr. Infect. Dis. 9(03), 127–134 (2014).
- 4. . Hospital epidemiology and infection control in acute-care settings. Clin. Microbiol. Rev. 24(1), 141–173 (2011).
- 5. . Antibiotic resistance threats in the United States. Centers Dis. Control Prev. 114, 11–89 (2013).
- 6. . Estimating the impact of antimicrobial resistance. Lancet Glob. Health 6(9), e934–e935 (2018). •• Highlights global estimates, the WHO's efforts and a global action plan to combat antimicrobial resistance.
- 7. . Mechanisms of antibiotic resistance. Microbiol. Spectr. 4(2), 15 (2016).
- 8. . Biofilms and device-related infections. In: Persistent Bacterial Infections. Nataro JPBlaser MJCunningham-Rundles S (Eds). ASM Press, WA, USA, 423–439 (2000).
- 9. Natural strategies as potential weapons against bacterial biofilms. Life 12(10), 1618 (2022).
- 10. . Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407(6805), 762–764 (2000). •• An important work that analyzed the role of biofilm in resistance to antibiotic therapy in Pseudomonas aeruginosa among patients with cystic fibrosis lungs.
- 11. The Immune Response to Bacterial Biofilms. Cambridge University Press, Cambridge, UK (1995).
- 12. . The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 37(6), 1771–1776 (1999). • Authors devised a new technology for rapid susceptibility analysis of microbial strains to antibiotics and biofilms. This may help researchers in the rational selection of antibiotics against biofilm-forming bacteria and for screening of new antimicrobial compounds.
- 13. . Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4(4), e1000052 (2008).
- 14. . Biofilm formation by staphylococci in health-related environments and recent reports on their control using natural compounds. Crit. Rev. Microbiol. 45(2), 201–222 (2019).
- 15. Potential of medicinal plants from the Brazilian semi-arid region (Caatinga) against Staphylococcus epidermidis planktonic and biofilm lifestyles. J. Ethnopharmacol. 137(1), 327–335 (2011).
- 16. Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Antimicrob. Agents Chemother. 56(5), 2314–2325 (2012).
- 17. A broad range quorum sensing inhibitor working through sRNA inhibition. Sci. Rep. 7(1), 1–12 (2017).
- 18. Allicin inhibits Pseudomonas aeruginosa virulence by suppressing the rhl and pqs quorum-sensing systems. Can. J. Microbiol. 65(8), 563–574 (2019).
- 19. Virulence of Pseudomonas aeruginosa exposed to carvacrol: alterations of the quorum sensing at enzymatic and gene levels. J. Cell Commun. Signal. 13(4), 531–537 (2019).
- 20. . The effect of emodin on Staphylococcus aureus strains in planktonic form and biofilm formation in vitro. Arch. Microbiol. 199(9), 1267–1275 (2017).
- 21. . Emodin, a natural inhibitor of protein kinase CK2, suppresses growth, hyphal development, and biofilm formation of Candida albicans. Yeast 34(6), 253–265 (2017).
- 22. Aloe-emodin inhibits Staphylococcus aureus biofilms and extracellular protein production at the initial adhesion stage of biofilm development. Appl. Microbiol. Biotechnol. 101(17), 6671–6681 (2017).
- 23. . Hordenine: a novel quorum sensing inhibitor and antibiofilm agent against Pseudomonas aeruginosa. J. Agric. Food Chem. 66(7), 1620–1628 (2018).
- 24. . Callistemon citrinus bioactive metabolites as new inhibitors of methicillin-resistant Staphylococcus aureus biofilm formation. J. Ethnopharmacol. 254, 112669 (2020).
- 25. Attenuation of Pseudomonas aeruginosa biofilm formation by vitexin: a combinatorial study with azithromycin and gentamicin. Sci. Rep. 6(1), 1–13 (2016).
- 26. . Piper betle and its bioactive metabolite phytol mitigates quorum sensing mediated virulence factors and biofilm of nosocomial pathogen Serratia marcescens in vitro. J. Ethnopharmacol. 193, 592–603 (2016).
- 27. . Isolimonic acid interferes with Escherichia coli O157: h7 biofilm and TTSS in QseBC and QseA dependent fashion. BMC Microbiol. 12(1), 1–13 (2012).
- 28. . Synthesis of (R)-norbgugaine and its potential as quorum sensing inhibitor against Pseudomonas aeruginosa. Bioorg. Med. Chem. Lett. 23(8), 2353–2356 (2013).
- 29. . Zingerone silences quorum sensing and attenuates virulence of Pseudomonas aeruginosa. Fitoterapia 102, 84–95 (2015).
- 30. Baicalin inhibits biofilm formation, attenuates the quorum sensing-controlled virulence and enhances Pseudomonas aeruginosa clearance in a mouse peritoneal implant infection model. PLOS ONE 12(4), e0176883 (2017).
- 31. . Antibiofilm and antivirulence efficacies of flavonoids and curcumin against Acinetobacter baumannii. Front. Microbiol. 10, 990 (2019).
- 32. . Inhibitory effects of myricetin derivatives on curli-dependent biofilm formation in Escherichia coli. Sci. Rep. 8(1), 8452 (2018).
- 33. Membrane-interactive compounds from Pistacia lentiscus L. thwart Pseudomonas aeruginosa virulence. Front. Microbiol. 11, 1068 (2020).
- 34. Efficacy of chelerythrine against mono-and dual-species biofilms of Candida albicans and Staphylococcus aureus and its properties of inducing hypha-to-yeast transition of C. albicans. J. Fungi 6(2), 45 (2020).
- 35. The chemical and antibacterial evaluation of St. John's Wort oil macerates used in Kosovar traditional medicine. Front. Microbiol. 8, 1639 (2017).
- 36. Biofilm inhibiting properties of compounds from the leaves of Warburgia ugandensis Sprague subsp ugandensis against Candida and staphylococcal biofilms. J. Ethnopharmacol. 248, 112352 (2020).
- 37. . Multiple roles of biosurfactants in biofilms. Curr. Pharm. Des. 22(11), 1429–1448 (2016).
- 38. Antimicrobial, anti-biofilm, and anti-proliferative activities of lipopeptide biosurfactant produced by Acinetobacter junii B6. Microb. Pathog. 138, 103806 (2020). • A biogenic biosurfactant isolated from Acinetobacter junii B6 strain, reported as an antimicrobial and antibiofilm agent.
- 39. . In vitro and Ex vivo antibiofilm activity of a lipopeptide biosurfactant produced by the entomopathogenic Beauveria bassiana strain against Microsporum canis. Microorganisms 8(2), 232 (2020).
- 40. . In vitro efficacy of the lipopeptide biosurfactant surfactin-C15 and its complexes with divalent counterions to inhibit Candida albicans biofilm and hyphal formation. Biofouling 36(2), 210–221 (2020).
- 41. Antibacterial, anti-adherent and cytotoxic activities of surfactin (s) from a lipolytic strain Bacillus safensis F4. Biodegradation 30(4), 287–300 (2019).
- 42. . Pontifactin, a new lipopeptide biosurfactant produced by a marine Pontibacter korlensis strain SBK-47: purification, characterization and its biological evaluation. Process Biochem. 51(12), 2198–2207 (2016).
- 43. . Lipopeptides from Bacillus subtilis AC7 inhibit adhesion and biofilm formation of Candida albicans on silicone. Antonie Van Leeuwenhoek 109(10), 1375–1388 (2016).
- 44. . Evaluation of anti-cancer, anti-microbial and anti-biofilm potential of biosurfactant extracted from an Acinetobacter M6 strain. J. King Saud. Univ. Sci. 32(1), 223–227 (2020).
- 45. . Characterization of biosurfactant produced by the endophyte Burkholderia sp. WYAT7 and evaluation of its antibacterial and antibiofilm potentials. J. Biotechnol. 313, 1–10 (2020).
- 46. Evaluation of anti-oxidant and anti-biofilm activities of biogenic surfactants derived from Bacillus amyloliquefaciens and Pseudomonas aeruginosa. Iran. J. Pharm. Sci. 19(2), 115 (2020).
- 47. . Rhamnolipids from non-pathogenic Burkholderia thailandensis E264: physicochemical characterization, antimicrobial and antibiofilm efficacy against oral hygiene related pathogens. New Biotechnol. 36, 26–36 (2017).
- 48. . Exopolysaccharides produced by Pandoraea shows emulsifying and anti-biofilm activities. J. Polym. Res. 26(4), 1–11 (2019).
- 49. Quantitative-HPLC-DAD polyphenols analysis, anxiolytic and cognition enhancing potentials of Sorbaria tomentosa Lindl. Rehder. J. Ethnopharmacol. 317, 116786 (2023).
- 50. Polyphenol-enriched Desmodium elegans DC. ameliorate scopolamine-induced amnesia in animal model of Alzheimer's disease: in vitro, in vivo and in silico approaches. Biomed. Pharmacother. 165, 115144 (2023).
- 51. . Dietary polyphenols and their biological significance. Int. J. Mol. Sci. 8(9), 950–988 (2007).
- 52. . Benefits of polyphenols on gut microbiota and implications in human health. J. Nutr. Biochem. 24(8), 1415–1422 (2013).
- 53. . Techniques for analysis of plant phenolic compounds. Molecules 18(2), 2328–2375 (2013).
- 54. . Polyphenols, dietary sources and bioavailability. Ann. Ist. Super. Sanita 43(4), 348 (2007).
- 55. . Health promoting and sensory properties of phenolic compounds in food. Rev. Ceres. 61, 764–779 (2014).
- 56. . Chemistry and biochemistry of dietary polyphenols. Nutrients 2(12), 1231–1246 (2010).
- 57. Mechanistic insights into the role of plant polyphenols and their nano-formulations in the management of depression. Front. Pharmacol. 13, 4731 (2022).
- 58. . Phenolics in human health. Int. J. Chem. Eng. Appl. 5(5), 393 (2014).
- 59. . Plant Secondary Metabolites: Occurrence, Structure and Role in the Human Diet. Blackwell Publishing Ltd, Oxford, UK (2008).
- 60. . Chapter: 50 phenolic compounds: introduction. Nat. Prod. 1543–1580 (2013).
- 61. . Phytochemicals as Nutraceuticals–Global Approaches to Their Role in Nutrition and Health. InTech, London, UK (2012).
- 62. . Progress on the chemistry of dibenzocyclooctadiene lignans. Chem. Rev. 105(12), 4581–4609 (2005).
- 63. . Phenolics: from chemistry to biology. Molecules 14(6), 2202–2211 (2009).
- 64. . Polyphenols as antimicrobial agents. Curr. Opin. Biotechnol. 23(2), 174–181 (2012).
- 65. . Natural products as antimicrobial agents. Food Control 46, 412–429 (2014).
- 66. . Plant natural products targeting bacterial virulence factors. Chem. Rev. 116(16), 9162–9236 (2016).
- 67. . Quorum quenching activity of Syzygium cumini (L.) Skeels and its anthocyanin malvidin against Klebsiella pneumoniae. Microb. Pathog. 79, 61–69 (2015).
- 68. . Deciphering the role of coumarin as a novel quorum sensing inhibitor suppressing virulence phenotypes in bacterial pathogens. Appl. Microbiol. Biotechnol. 99(7), 3303–3316 (2015). • Reports the role of coumarin as an inhibitor of quorum sensing with subsequent inhibition of biofilm formation.
- 69. Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 79(1), 119–126 (2008).
- 70. . Coumarins reduce biofilm formation and the virulence of Escherichia coli O157: h7. Phytomedicine 21(8–9), 1037–1042 (2014).
- 71. Screening for novel quorum-sensing inhibitors to interfere with the formation of Pseudomonas aeruginosa biofilm. J. Med. Microbiol. 60(12), 1827–1834 (2011).
- 72. . Systematic exploration of natural and synthetic flavonoids for the inhibition of Staphylococcus aureus biofilms. Int. J. Mol. Sci. 14(10), 19434–19451 (2013).
- 73. Molecular basis of Streptococcus mutans sortase A inhibition by the flavonoid natural product trans-chalcone. Chem. Comm. 51(52), 10483–10485 (2015).
- 74. Antiadherent and antibiofilm activity of Humulus lupulus L. derived products: new pharmacological properties. Biomed Res. Int. 2013, 101089 (2013).
- 75. . Suppression of bacterial cell–cell signalling, biofilm formation and type III secretion system by citrus flavonoids. J. Appl. Microbiol. 109(2), 515–527 (2010).
- 76. . Red wines and flavonoids diminish Staphylococcus aureus virulence with anti-biofilm and anti-hemolytic activities. Biofouling 31(1), 1–11 (2015).
- 77. . Chemoinformatics-assisted development of new anti-biofilm compounds. Appl. Microbiol. Biotechnol. 87(1), 309–317 (2010).
- 78. . Inhibition of Escherichia coli O157: h7 motility and biofilm by β-sitosterol glucoside. Biochim. Biophys. Acta Gen. Subj. 1830(11), 5219–5228 (2013).
- 79. . Guaijaverin–a plant flavonoid as potential antiplaque agent against Streptococcus mutans. J. Appl. Microbiol. 101(2), 487–495 (2006).
- 80. . Inhibition of major virulence pathways of Streptococcus mutans by quercitrin and deoxynojirimycin: a synergistic approach of infection control. PLOS ONE 9(3), e91736 (2014).
- 81. . Polyphenolic extract from Rosa rugosa tea inhibits bacterial quorum sensing and biofilm formation. Food Control 42, 125–131 (2014).
- 82. Apple flavonoid phloretin inhibits Escherichia coli O157: h7 biofilm formation and ameliorates colon inflammation in rats. Infect. Immun. 79(12), 4819–4827 (2011).
- 83. . Morin inhibits biofilm production and reduces the virulence of Listeria monocytogenes–An in vitro and in vivo approach. Int. J. Food Microbiol. 237, 73–82 (2016).
- 84. . Effects of Epigallocatechin gallate against Enterococcus faecalis biofilm and virulence. Arch. Oral Biol. 60(3), 393–399 (2015).
- 85. Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 76(1), 243–253 (2010).
- 86. . Inhibitory effect of methyl gallate and gallic acid on oral bacteria. J. Microbiol. 46(6), 744–750 (2008).
- 87. Inhibition of gallic acid on the growth and biofilm formation of Escherichia coli and Streptococcus mutans. J. Food Sci. 80(6), M1299–M1305 (2015).
- 88. . Inhibitory effects of 1, 2, 3, 4, 6-penta-O-galloyl-β-D-glucopyranose on biofilm formation by Staphylococcus aureus. Antimicrob. Agents Chemother. 55(3), 1021–1027 (2011).
- 89. . Dietary plant components ellagic acid and tannic acid inhibit Escherichia coli biofilm formation. J. Med. Microbiol. 59(4), 496 (2010).
- 90. . Lycopus europaeus: phenolic fingerprint, antioxidant activity and antimicrobial effect on clinical Staphylococcus aureus strains. Nat. Prod. Res. 29(24), 2271–2274 (2015).
- 91. . Membrane active antimicrobial peptides: translating mechanistic insights to design. Front. Neurosci. 11, 73 (2017).
- 92. . Lantibiotics: mode of action, biosynthesis and bioengineering. Curr. Pharm. Biotechnol. 10(1), 2–18 (2009).
- 93. . Molecular mechanism of target recognition by subtilin, a class I lanthionine antibiotic. Antimicrob. Agents Chemother. 52(2), 612–618 (2008).
- 94. The nisin–lipid II complex reveals a pyrophosphate cage that provides a blueprint for novel antibiotics. Nat. Struct. Mol. Biol. 11(10), 963–967 (2004).
- 95. . Sophorolipid biosurfactants: possible uses as antibacterial and antibiofilm agent. New Biotechnol. 32(6), 720–726 (2015).
- 96. . A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135(3), 486–496 (2008).
- 97. . Rapid degradation of Streptococcus pyogenes biofilms by PlyC, a bacteriophage-encoded endolysin. J. Antimicrob. Chemother. 68(8), 1818–1824 (2013).
- 98. . Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens. Int. J. Med. Microbiol. 300(6), 357–362 (2010).
- 99. . Biofilms and their consequences, with particular reference to hygiene in the food industry. J. Appl. Bacteriol. 75(6), 499–511 (1993).
- 100. . The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochem. 40(10), 3016–3026 (2001).
- 101. . Structures of proline-rich peptides bound to the ribosome reveal a common mechanism of protein synthesis inhibition. Nucleic Acids Res. 44(5), 2439–2450 (2016).
- 102. . Staphylococcal biofilm disassembly. Trends Microbiol. 19(9), 449–455 (2011).
- 103. . Enzymatic degradation of biofilm by metalloprotease from microbacterium sp. SKS10. Front. Bioeng. Biotechnol. 7, 192 (2019).
- 104. . Peptide signaling in the staphylococci. Chem. Rev. 111(1), 117–151 (2011).
- 105. Epistatic relationships between sarA and agr in Staphylococcus aureus biofilm formation. PLOS ONE 5(5), e10790 (2010).
- 106. . Will biofilm disassembly agents make it to market? Trends Microbiol. 19(7), 304–306 (2011).
- 107. . Antibiofilm polysaccharides. Environ. Microbiol. 15(2), 334–346 (2013).
- 108. Antibiofilm activity of an exopolysaccharide from marine bacterium Vibrio sp. QY101. PLOS ONE 6(4), e18514 (2011).
- 109. . Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLOS ONE 7(10), e46718 (2012).
- 110. . Antibiofilm and anti-infection of a marine bacterial exopolysaccharide against Pseudomonas aeruginosa. Front. Microbiol. 7, 102 (2016).
- 111. . Prospects for anti-biofilm pharmaceuticals. Pharmaceuticals 8(3), 504–511 (2015).
- 112. . Therapeutic potential of biofilm-dispersing enzymes. Int. J. Artif. Organs 32(9), 545–554 (2009).
- 113. Inhibiting bacterial cooperation is an evolutionarily robust anti-biofilm strategy. Nat. Commun. 11(1), 1–11 (2020).
- 114. . Molecular mechanisms that confer antibacterial drug resistance. Nature 406(6797), 775–781 (2000).
- 115. . Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44(7), 1818–1824 (2000).
- 116. . The effects of adherence to silicone surfaces on antibiotic susceptibility in Staphylococcus aureus. Microbiology 143(7), 2407–2413 (1997).
- 117. . Theoretical aspects of antibiotic diffusion into microbial biofilms. Antimicrob. Agents Chemother. 40(11), 2517–2522 (1996).
- 118. . A review of experimental measurements of effective diffusive permeabilities and effective diffusion coefficients in biofilms. Biotechnol. Bioeng. 59(3), 261–272 (1998).
- 119. . Permeation of antimicrobial agents through Pseudomonas aeruginosa biofilms: a simple method. Chemotherapy 43(5), 340–345 (1997).
- 120. . Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol. Bioeng. 43(11), 1131–1138 (1994).
- 121. . Evaluation of substrate and pH effects in a nitrifying biofilm. Water Environ. Res. 68(7), 1107–1115 (1996).
- 122. . Increased minimum inhibitory concentrations with anaerobiasis for tobramycin, gentamicin, and amikacin, compared to latamoxef, piperacillin, chloramphenicol, and clindamycin. Chemotherapy 31(3), 204–210 (1985).
- 123. . The rate of killing of Escherichia coli by β-lactam antibiotics is strictly proportional to the rate of bacterial growth. Microbiology 132(5), 1297–1304 (1986).
- 124. . Reduced susceptibility of thin Pseudomonas aeruginosa biofilms to hydrogen peroxide and monochloramine. J. Appl. Microbiol. 88(1), 22–30 (2000).
- 125. . Biosynthesized metallic nanoparticles as emerging cancer theranostics agents. In: Nanotheranostics, Springer, 229–244 (2019).
- 126. Floral extracts-mediated green synthesis of NiO nanoparticles and their diverse pharmacological evaluations. J. Biomol. Struct. Dyn. 39(11), 4133–4147 (2021).
- 127. In-depth in-vitro and in-vivo anti-diabetic evaluations of Fagonia cretica mediated biosynthesized selenium nanoparticles. Biomed. Pharmacother. 164, 114872 (2023).
- 128. Research progress of polyphenols in nanoformulations for antibacterial application. Mater. Today Bio. 21, 100729 (2023).
- 129. . Designing hydrogels for controlled drug delivery. Nat. Rev. Mater. 1(12), 1–17 (2016).
- 130. . Characterisation of hydrogels: linking the nano to the microscale. Adv. Colloid Interface Sci. 274, 102044 (2019).
- 131. . Lipid-based nanoparticle formulations for small molecules and RNA drugs. Expert Opin. Drug Deliv. 16(11), 1205–1226 (2019).
- 132. . Liposomes: from a clinically established drug delivery system to a nanoparticle platform for theranostic nanomedicine. Acc. Chem. Res. 44(10), 1094–1104 (2011).
- 133. . Nanofiber systems as herbal bioactive compounds carriers: current applications in healthcare. Pharmaceutics 14(1), 191 (2022).
- 134. . Functionalized PVA–silk blended nanofibrous mats promote diabetic wound healing via regulation of extracellular matrix and tissue remodelling. J. Tissue Eng. Regen. Med. 12(3), e1559–e1570 (2018).
- 135. Nano-based drug delivery systems: recent developments and future prospects. J. Nanobiotechnology 16(1), 1–33 (2018).
- 136. . Twin peaks: presenting the antagonistic molecular interplay of curcumin with LasR and LuxR quorum sensing pathways. Curr. Microbiol. 77(8), 1800–1810 (2020).
- 137. . Curcumin induced photodynamic therapy mediated suppression of quorum sensing pathway of Pseudomonas aeruginosa: an approach to inhibit biofilm in vitro. Photodiagnosis Photodyn. Ther. 30, 101645 (2020).
- 138. . Sustained release curcumin loaded solid lipid nanoparticles. Adv. Pharm. Bull. 6(1), 17 (2016).
- 139. . Chinese white wax solid lipid nanoparticles as a novel nanocarrier of curcumin for inhibiting the formation of Staphylococcus aureus biofilms. Nanomaterials 9(5), 763 (2019).
- 140. . Gelucire-based nanoparticles for curcumin targeting to oral mucosa: preparation, characterization, and antimicrobial activity assessment. J. Pharm. Sci. 104(11), 3913–3924 (2015).
- 141. . Preparation and antibiofilm studies of curcumin loaded chitosan nanoparticles against polymicrobial biofilms of Candida albicans and Staphylococcus aureus. Carbohydr. Polym. 241, 116254 (2020).
- 142. . Acceleration of antibacterial activity of curcumin loaded biopolymers against methicillin-resistant Staphylococcus aureus: synthesis, optimization, and evaluation. Eng. Life Sci. 22(2), 58–69 (2022).
- 143. Encapsulation of curcumin in polymeric nanoparticles for antimicrobial photodynamic therapy. PLOS ONE 12(11), e0187418 (2017).
- 144. . Synergistic antibacterial effects of curcumin modified silver nanoparticles through ROS-mediated pathways. Mater. Sci. Eng. C 99, 255–263 (2019).
- 145. Combination of silver nanoparticles and curcumin nanoparticles for enhanced anti-biofilm activities. J. Agric. Food Chem. 64(12), 2513–2522 (2016).
- 146. . Mesoporous silica nanoparticles: a comprehensive review on synthesis and recent advances. Pharmaceutics 10(3), 118 (2018).
- 147. . Fabrication and characterization of PCL/gelatin/curcumin nanofibers and their antibacterial properties. J. Ind. Text. 46(2), 562–577 (2016).
- 148. . Nanoemulsions of green tea catechins and other natural compounds for the treatment of urinary tract infection: antibacterial analysis. Adv. Pharm. Bull. 9(3), 401 (2019).
- 149. . Antibacterial effects of curcumin encapsulated in nanoparticles on clinical isolates of Pseudomonas aeruginosa through downregulation of efflux pumps. Mol. Biol. Rep. 46, 2395–2404 (2019).
- 150. . Synthesis and self-assembly of curcumin-modified amphiphilic polymeric micelles with antibacterial activity. J. Nanobiotechnology 19(1), 1–15 (2021).
- 151. . Combinatorial liposomes of berberine and curcumin inhibit biofilm formation and intracellular methicillin-resistant Staphylococcus aureus infections and associated inflammation. J. Mater. Chem. B 9(3), 864–875 (2021).
- 152. Evaluation ofnano-curcumin effects on expression levels of virulence genes and biofilm production of multidrug-resistant Pseudomonas aeruginosa isolated from burn wound infection in Tehran, Iran. Infect. Drug Resist. 12, 2223–2235 (2019).
- 153. Curcumin quantum dots mediated degradation of bacterial biofilms. Front. Microbiol. 8, 1517 (2017).
- 154. . Preparation of epigallocatechin gallate-loaded nanoparticles and characterization of their inhibitory effects on Helicobacter pylori growth in vitro and in vivo. Sci. Technol. Adv. Mater. 15(4), 045006 2014).
- 155. High antibacterial in vitro performance of gold nanoparticles synthesized by epigallocatechin 3-gallate. J. Mater. Res. 36, 518–532 (2021).
- 156. . DNA functionalized metal and metal oxide nanoparticles: principles and recent advances in food safety detection. Crit. Rev. Food Sci. Nutr. 61(14), 2277–2296 (2021).
- 157. Polyphenol-binding amyloid fibrils self-assemble into reversible hydrogels with antibacterial activity. ACS Nano 12(4), 3385–3396 (2018).
- 158. EGCG-coated silver nanoparticles self-assemble with selenium nanowires for treatment of drug-resistant bacterial infections by generating ROS and disrupting biofilms. Nanotechnology 33(41), 415101 (2022).
- 159. . Antimicrobial activity of quercetin: an approach to its mechanistic principle. Molecules 27(8), 2494 (2022).
- 160. . Synergic formulation of onion peel quercetin loaded chitosan-cellulose hydrogel with green zinc oxide nanoparticles towards controlled release, biocompatibility, antimicrobial and anticancer activity. Int. J. Biol. Macromol. 132, 784–794 (2019).
- 161. Preparation, characterization, and enhanced antimicrobial activity: quercetin-loaded PLGA nanoparticles against foodborne pathogens. Turk. J. Biol. 41(1), 127–140 (2017).
- 162. . Preparation and evaluation of mesoporous silica nanoparticles loaded quercetin against bacterial infections in Oreochromis niloticus. Aquac. Rep. 21, 100808 (2021).
- 163. . Biosynthesis, characterization of silver nanoparticles using quercetin from Clitoria ternatea L to enhance toxicity against bacterial biofilm. J. Inorg. Organomet. Polym. Mater. 27(5), 1412–1422 (2017).
- 164. The anti-biofilm effect of silver-nanoparticle-decorated quercetin nanoparticles on a multi-drug resistant Escherichia coli strain isolated from a dairy cow with mastitis. PeerJ 6, e5711 (2018).
- 165. Quorum quenching of Streptococcus mutans via the nano-quercetin-based antimicrobial photodynamic therapy as a potential target for cariogenic biofilm. BMC Microbiol. 22(1), 125 (2022).
- 166. . A Potential quorum-sensing inhibitor for bronchiectasis therapy: quercetin–chitosan nanoparticle complex exhibiting superior inhibition of biofilm formation and swimming motility of Pseudomonas aeruginosa to the native quercetin. Int. J. Mol. Sci. 22(4), 1541 (2021).
- 167. . Anti-biofilm activities of quercetin and tannic acid against Staphylococcus aureus. Biofouling 29(5), 491–499 (2013).
- 168. A biocompatible bacterial cellulose/tannic acid composite with antibacterial and anti-biofilm activities for biomedical applications. Mater. Sci. Eng. C 106, 110249 (2020).
- 169. . Self-assembly of metal–phenolic networks as functional coatings for preparation of antioxidant, antimicrobial, and pH-sensitive-modified starch nanoparticles. ACS Sustain. Chem. Eng. 7(20), 17379–17389 (2019).
- 170. . Multifunctional and recyclable photothermally responsive cryogels as efficient platforms for wound healing. Adv. Funct. Mater. 29(35), 1904402 (2019).
- 171. Biodegradable hydrogel with thermo-response and hemostatic effect for photothermal enhanced anti-infective therapy. Nano Today 39, 101165 (2021).
- 172. . Antibacterial and anti-inflammatory pH-responsive tannic acid-carboxylated agarose composite hydrogels for wound healing. ACS Appl. Mater. Interfaces 8(42), 28511–28521 (2016).
- 173. Multistage ROS-responsive and natural polyphenol-driven prodrug hydrogels for diabetic wound healing. ACS Appl. Mater. Interfaces 14(47), 52643–52658 (2022).
- 174. Tannic acid-modified silver nanoparticles for enhancing anti-biofilm activities and modulating biofilm formation. Biomater. Sci. 8(17), 4852–4860 (2020).
- 175. . Optimization and characterization of tannic acid loaded niosomes for enhanced antibacterial and anti-biofilm activities. Adv. Powder Technol. 31(12), 4768–4781 (2020).
- 176. . Antimicrobial and antibiofilm activity of GNP-tannic acid-Ag nanocomposite and their epoxy-based coatings. Prog. Org. Coat. 159, 106421 (2021).
- 177. . Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb. Drug Resist. 19(4), 256–265 (2013).
- 178. . Functionalized ZnO nanoparticles with gallic acid for antioxidant and antibacterial activity against methicillin-resistant S. aureus. Nanomaterials 7(11), 365 (2017).
- 179. Two choices for the functionalization of silica nanoparticles with gallic acid: characterization of the nanomaterials and their antimicrobial activity against Paenibacillus larvae. J. Nanopart. Res. 18, 1–13 (2016).
- 180. . Evaluation of the antibacterial activity of gallic acid anchored phthalocyanine-doped silica nanoparticles towards Escherichia coli and Staphylococcus aureus biofilms and planktonic cells. Photodiagnosis Photodyn. Ther. 42, 103520 (2023).
- 181. . Gelatin–gallic acid microcomplexes release GO/Cu nanomaterials to eradicate antibiotic-resistant microbes and their biofilm. ACS Infect. Dis. 9(2), 296–307 (2023).
- 182. Bifunctional viscous nanovesicles co-loaded with resveratrol and gallic acid for skin protection against microbial and oxidative injuries. Eur. J. Pharm. Biopharm. 114, 278–287 (2017).
- 183. A comprehensive study on the antimicrobial properties of resveratrol as an alternative therapy. Evid. Based Complement. Alternat. Med. 2021, 8866311 (2021).
- 184. . Resveratrol nanoformulations: challenges and opportunities. Int. J. Pharm. 479(2), 282–290 (2015).
- 185. Antibacterial nanocarriers of resveratrol with gold and silver nanoparticles. Mater. Sci. Eng. C 58, 1160–1169 (2016).
- 186. . Preparation, characterization and antimicrobial activity evaluation of electrospun PCL nanofiber composites of resveratrol nanocrystals. Pharm. Dev. Technol. 25(10), 1216–1225 (2020).
- 187. Multicomponent antibiofilm lipid nanoparticles as novel platform to ameliorate resveratrol properties: preliminary outcomes on fibroblast proliferation and migration. Int. J. Mol. Sci. 24(9), 8382 (2023).
- 188. Mannosyl, glucosyl or galactosyl liposomes to improve resveratrol efficacy against methicillin resistant Staphylococcus aureus biofilm. Colloids Surf. A Physicochem. Eng. Asp. 617, 126321 (2021).
- 189. Co-delivery of diverse therapeutic compounds using PEG–PLGA nanoparticle cargo against drug-resistant bacteria: an improved anti-biofilm strategy. ACS Appl. Bio Mater. 3(1), 385–399 (2019).
- 190. Bioflavonoid mediated synthesis of TiO2 nanoparticles: characterization and their biomedical applications. Mater. Lett. 311, 131639 (2022).
- 191. Co-delivery of diverse therapeutic compounds using PEG–PLGA nanoparticle cargo against drug-resistant bacteria: an improved anti-biofilm strategy. ACS Appl. Bio Mater. 3(1), 385–399 (2020).
- 192. . Chitosan/cyclodextrin surface-adsorbed naringenin-loaded nanocapsules enhance bacterial quorum quenching and anti-biofilm activities. Colloids Surf. B Biointerfaces 211, 112281 (2022).
- 193. . Facile green synthesis of baicalein fabricated gold nanoparticles and their antibiofilm activity against Pseudomonas aeruginosa PAO1. Microb. Pathog. 107, 261–269 (2017).
- 194. Co-delivery of antibiotic and baicalein by using different polymeric nanoparticle cargos with enhanced synergistic antibacterial activity. Int. J. Pharm. 599, 120419 (2021).
- 195. Scaffold of selenium nanovectors and honey phytochemicals for inhibition of Pseudomonas aeruginosa quorum sensing and biofilm formation. Front. Cell. Infect. Microbiol. 7, 93 (2017).
- 196. Chrysin-loaded chitosan nanoparticles potentiates antibiofilm activity against Staphylococcus aureus. Pathogens 9(2), 115 (2020).
- 197. . Chitosan nanoparticles enhances the anti-quorum sensing activity of kaempferol. Int. J. Biol. Macromol. 94, 653–662 (2017).
- 198. . Ferulic acid encapsulated chitosan-tripolyphosphate nanoparticles attenuate quorum sensing regulated virulence and biofilm formation in Pseudomonas aeruginosa PAO1. IET Nanobiotechnol. 12(8), 1056–1061 (2018).