The activity of ferulic and gallic acids in biofilm prevention and control of pathogenic bacteria

Biofouling

Volumn 28, Issue 7, 2012, Pages 755-767

  Borges, Anabela ^a,b   Saavedra, Maria J ^b   Simões, Manuel ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

Author keywords

biofilm control; biofilm prevention; ferulic acid; gallic acid; motility; pathogenic bacteria

Indexed keywords

ANTIINFECTIVE AGENT; COUMARIC ACID; FERULIC ACID; GALLIC ACID;

ADHESION; BACTERIUM; BIOFILM; CHEMICAL CONTROL; MOTILITY; PATHOGENICITY; PHENOLIC COMPOUND; PHYTOCHEMISTRY; SWARMING; SWIMMING;

ARTICLE; BACTERIUM ADHERENCE; BIOFILM; DOSE RESPONSE; DRUG EFFECT; ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BIOFILMS; COUMARIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; GALLIC ACID; LISTERIA MONOCYTOGENES; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

EID: 84864539034     PISSN: 08927014     EISSN: 10292454     Source Type: Journal    
DOI: 10.1080/08927014.2012.706751     Document Type: Article

References (101)

1. Ahmad, I and Aqil, F. 2007. In vitro efficacy of bioactive extracts of 15 medicinal plants against ES[beta]L-producing multidrug-resistant enteric bacteria. Microbiol Res, 162: 264-275.
2. Aires, A, Mota, VR, Saavedra, MJ, Rosa, EAS and Bennett, RN. 2009b. The antimicrobial effects of glucosinolates and their respective enzymatic hydrolysis products on bacteria isolated from the human intestinal tract. J Appl Microbiol, 106: 2086-2095.
3. Aires, A, Mota, VR, Saavedra, MJ, Monteiro, AA, Sim[otilde]es, M, Rosa, EAS and Bennett, RN. 2009a. Initial in vitro evaluations of the antibacterial activities of glucosinolate enzymatic hydrolysis products against plant pathogenic bacteria. J Appl Microbiol, 106: 2096-2105.
4. Al-Sohaibani, S and Murugan, K. 2012. Anti-biofilm activity of Salvadora persica on cariogenic isolates of Streptococcus mutans: in vitro and molecular docking studies. Biofouling, 28: 29-38.
5. An, YH and Friedman, RJ. 1998. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J Biomed Mater Res, 43: 338-348.
6. Anderson, GG and O'Toole, GA. 2008. Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol, 322: 85-105.
7. Aslam, S. 2008. Effect of antibacterials on biofilms. Am J Infect Control, 36: S175.e179-S175.e111.
8. Bennett, SM, Finlay, JA, Gunari, N, Wells, DD, Meyer, AE, Walker, GC, Callow, ME, Callow, JA, Bright, FV and Detty, MR. 2009. The role of surface energy and water wettability in aminoalkyl/fluorocarbon/hydrocarbon-modified xerogel surfaces in the control of marine biofouling. Biofouling, 26: 235-246.
9. Busscher, HJ, Weerkamp, AH and Van der Mei, HC. 1984. Measurement of the surface free energy of bacterial cell surfaces and its relevance for adhesion. Appl Environ Microbiol, 48: 980-983.
10. Butler, MT, Wang, Q and Harshey, RM. 2010. Cell density and mobility protect swarming bacteria against antibiotics. P Natl Acad Sci USA, 107: 3776-3781.
11. Campos, FM, Couto, JA, Figueiredo, AR, Tóth IV, Rangel, AOSS and Hogg, TA. 2009. Cell membrane damage induced by phenolic acids on wine lactic acid bacteria. Int J Food Microbiol, 135: 144-151.
12. Chen, X and Stewart, PS. 2000. Biofilm removal caused by chemical treatments. Water Res, 34: 4229-4233.
13. Cowan, MM. 1999. Plant products as antimicrobial agents. Clin Microbiol Rev, 12: 564-582.
14. Cushnie, TPT and Lamb, AJ. 2005. Antimicrobial activity of flavonoids. Int J Antimicrob Agents, 26: 343-356.
15. Daglia, M, Tarsi, R, Papetti, A, Grisoli, P, Dacarro, C, Pruzzo, C and Gazzani, G. 2002. Antiadhesive effect of green and roasted coffee on Streptococcus mutans adhesive properties on saliva-coated hydroxyapatite beads. J Agricult Food Chem, 50: 1225-1229.
16. Davies, D. 2003. Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov, 2: 114-122.
17. Déziel, E, Comeau, Y and Villemur, R. 2001. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol, 183: 1195-1204.
18. Dixon, RA. 2001. Natural products and plant disease resistance. Nature, 411: 843-847.
19. Donlan, RM and Costerton, JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev, 15: 167-193.
20. Drenkard, E. 2003. Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes Infect, 5: 1213-1219.
21. Ellnain-Wojtaszek, M and Lirska, I. 1998. Phenolic acids from Ginkgo biloba L. Part III. Antimicrobial activity of phenolic acids. Acta Pol Pharm, 55: 81-84.
22. Ergün, BC, Çoban, T, Onurdag, FK and Banoglu, E. 2011. Synthesis, antioxidant and antimicrobial evaluation of simple aromatic esters of ferulic acid. Arch Pharm Res, 34: 1251-1261.
23. Ferreira, C, Pereira, AM, Pereira, MC, Melo, LF and Sim[otilde]es, M. 2011. Physiological changes induced by the quaternary ammonium compound benzyldimethyldodecylammonium chloride on Pseudomonas fluorescens. J Antimicrob Chemother, 66: 1036-1043.
24. Furiga, A, Lonvaud-Funel, A, Dorignac, G and Badet, C. 2008. In vitro anti-bacterial and anti-adherence effects of natural polyphenolic compounds on oral bacteria. J Appl Microbiol, 105: 1470-1476.
25. Genzer, J and Efimenko, K. 2006. Recent developments in superhydrophobic surfaces and their relevance to marine fouling: a review. Biofouling, 22: 339-360.
26. Gilbert, P, McBain, AJ and Rickard, AH. 2003. Formation of microbial biofilm in hygienic situations: a problem of control. Int Biodeterior Biodegr, 51: 245-248.
27. Gómez-Gómez, JM, Manfredi, C, Alonso, JC and Blázquez, J. 2007. A novel role for RecA under non-stress: promotion of swarming motility in Escherichia coli K-12. BMC Biol, 5: 1-14.
28. Gray, MJ, Freitag, NE and Boor, KJ. 2006. How the bacterial pathogen Listeria monocytogenes mediates the switch from environmental Dr Jekyll to pathogenic Mr Hyde. Infect Immun, 74: 2506-2512.
29. Gründling, A, Burrack, LS, Bouwer, HGA and Higgins, DE. 2004. Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. P Natl Acad Sci USA, 101: 12318-12323.
30. Hancock, V, Dahl, M and Klemm, P. 2010. Abolition of biofilm formation in urinary tract Escherichia coli and Klebsiella isolates by metal interference through competition for fur. Appl Environ Microbiol, 76: 3836-3841.
31. Harshey, RM. 1994. Bees aren't the only ones: swarming in Gram-negative bacteria. Mol Microbiol, 13: 389-394.
32. Harshey, RM. 2003. Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol, 57: 249-273.
33. Hemaiswarya, S, Kruthiventi, AK and Doble, M. 2008. Synergism between natural products and antibiotics against infectious diseases. Phytomedicine, 15: 639-652.
34. Henrichsen, J. 1972. Bacterial surface translocation: a survey and a classification. Bacteriol Rev, 36: 478-503.
35. Huber, B, Eberl, L, Feucht, W and Polster, J. 2003. Influence of polyphenols on bacterial biofilm formation and quorum-sensing. Z Naturforsch, 58c: 874-884.
36. Inoue, T, Shingaki, R and Fukui, K. 2008. Inhibition of swarming motility of Pseudomonas aeruginosa by branched-chain fatty acids. FEMS Microbiol Lett, 281: 81-86.
37. Inoue, T, Shingaki, R, Hirose, S, Waki, K, Mori, H and Fukui, K. 2007. Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J Bacteriol, 189: 950-957.
38. Jagani, S, Chelikani, R and Kim, DS. 2009. Effects of phenol and natural phenolic compounds on biofilm formation by Pseudomonas aeruginosa. Biofouling, 25: 321-324.
39. Janczuk, B, Chibowski, E, Bruque, JM, Kerkeb, ML and Caballero, FG. 1993. On the consistency of surface free energy components as calculated from contact angles of different liquids: an application to the cholesterol surface. J Colloid Interf Sci, 159: 421-428.
40. Jarrell, KF and McBride, MJ. 2008. The surprisingly diverse ways that prokaryotes move. Nat Rev Microbiol, 6: 466-476.
41. Julkowska, D, Obuchowski, M, Holland, IB and Séror SJ. 2004. Branched swarming patterns on synthetic medium formed by wild-type Bacillus subtilis strain 3610: detection of different cellular morphologies and constellations of cells as the complex architecture develops. Microbiology, 150: 1839-1849.
42. Kaito, C and Sekimizu, K. 2007. Colony spreading in Staphylococcus aureus. J Bacteriol, 189: 2553-2557.
43. Kang, MS, Oh, JS, Kang, IC, Hong, SJ and Choi, CH. 2008. Inhibitory effect of methyl gallate and gallic acid on oral bacteria. J Microbiol, 46: 744-750.
44. Karatan, E and Watnick, P. 2009. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol R, 73: 310-347.
45. Kearns, DB, Robinson, J and Shimkets, LJ. 2001. Pseudomonas aeruginosa exhibits directed twitching motility up phosphatidylethanolamine gradients. J Bacteriol, 183: 763-767.
46. Kubo, I, Fujita, KI and Nihei, KI. 2003. Molecular design of multifunctional antibacterial agents against methicillin resistant Staphylococcus aureus (MRSA). Bioorg Med Chem Lett, 11: 4255-4262.
47. Kubo, I, Masuoka, N, Ha, TJ and Tsujimoto, K. 2006. Antioxidant activity of anacardic acids. Food Chem, 99: 555-562.
48. Lai, S, Trembaly, J and Déziel, E. 2009. Swarming motility: a multicellular behaviour conferring antimicrobial resistance. Environ Microbiol, 11: 126-136.
49. Lin, FH, Lin, JY, Gupta, RD, Tournas, JA, Burch, JA, Selim, MA, Monteiro-Riviere, NA, Grichnik, JM, Zielinski, J and Pinnell, SR. 2005. Ferulic acid stabilizes a solution of vitamins C and E and doubles its photoprotection of skin. J Invest Dermatol, 125: 826-832.
50. Machado, I, Graça, J, Sousa, AM, Lopes, SP and Pereira, MO. 2011. Effect of antimicrobial residues on early adhesion and biofilm formation by wild-type and benzalkonium chloride-adapted Pseudomonas aeruginosa. Biofouling, 27: 1151-1159.
51. Mah, TFC and O'Toole, GA. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol, 9: 34-39.
52. Manach, C, Scalbert, A, Morand, C, Rémésy, C and Jiménez, L. 2004. Polyphenols: food sources and bioavailability. Am J Clin Nutr, 79: 727-747.
53. Morton, LW, Abu-Amsha Caccetta, R, Puddey, IB and Croft, KD. 2000. Chemistry and biological effects of dietary phenolic compounds: relevance to cardiovascular disease. Clin Exp Pharmacol Physiol, 27: 152-159.
54. Muthuswamy, S and Rupasinghe, HPV. 2007. Fruit phenolics as natural antimicrobial agents: selective antimicrobial activity of catechin, chlorogenic acid and phloridzin. J Food Agric Environ, 5: 81-85.
55. O'Toole, GA and Kolter, R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol, 30: 295-304.
56. Overhage, J, Lewenza, S, Marr, AK and Hancock, REW. 2007. Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol, 189: 2164-2169.
57. Overhage, J, Bains, M, Brazas, MD and Hancock, REW. 2008. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol, 190: 2671-2679.
58. Pettit, RK, Weber, CA and Pettit, GR. 2009. Application of a high throughput Alamar blue biofilm susceptibility assay to Staphylococcus aureus biofilms. Ann Clin Microbiol Antimicrob, 8: 28
59. Phan, TT, Wang, L, See, P, Grayer, RJ, Chan, SY and Lee, ST. 2001. Phenolic compounds of Chromolaena odorata protect cultured skin cells from oxidative damage: implication for cutaneous wound healing. Biol Pharm Bull, 24: 1373-1379.
60. Pratt, LA and Kolter, R. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol, 30: 285-293.
61. Prior, RL and Cao, G. 2000. Antioxidant phytochemicals in fruits and vegetables: diet and health implications. HortScience, 35: 588-592.
62. Puupponen-Pimiä, R, Nohynek, L, Alakomi, HL and Oksman-Caldentey, KM. 2005. Bioactive berry compounds-novel tools against human pathogens. Appl Microbiol Biotechnol, 67: 8-18.
63. Rashid, MH and Kornberg, A. 2000. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. P Natl Acad Sci USA, 97: 4885-4890.
64. Robbins, RJ. 2003. Phenolic acids in foods: an overview of analytical methodology. J Agric Food Chem, 51: 2866-2887.
65. Roberts, AJ, Williams, SK, Wiedmann, M and Nightingale, KK. 2009. Some Listeria monocytogenes outbreak strains demonstrate significantly reduced invasion, inlA transcript levels, and swarming motility in vitro. Appl Environ Microbiol, 75: 5647-5658.
66. Saavedra, MJ, Borges, A, Dias, C, Aires, A, Bennett, RN, Rosa, ES and Sim[otilde]es, M. 2010. Antimicrobial activity of phenolics and glucosinolate hydrolysis products and their synergy with streptomycin against pathogenic bacteria. Med Chem, 6: 174-183.
67. Sakagami, H, Oi, T and Satoh, K. 1999. Prevention of oral diseases by polyphenols (review). In Vivo, 13: 155-171.
68. Samy, RP and Gopalakrishnakone, P. 2010. Therapeutic potential of plants as anti-microbials for drug discovery. Evid Based Complement Alternat Med, 7: 283-294.
69. Sarker, SD, Nahar, L and Kumarasamy, Y. 2007. Microtitre plate-based antibacterial assay incorporating resazurin as an indicator of cell growth, and its application in the in vitro antibacterial screening of phytochemicals. Methods, 42: 321-324.
70. Scalbert, A. 1991. Antimicrobial properties of tannins. Phytochemistry, 30: 3875-3883.
71. Sendamangalam, V, Choi, OK, Kim, D and Seo, Y. 2011. The anti-biofouling effect of polyphenols against Streptococcus mutans. Biofouling, 27: 13-19.
72. Shrout, JD, Chopp, DL, Just, CL, Hentzer, M, Givskov, M and Parsek, MR. 2006. The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional. Mol Microbiol, 62: 1264-1277.
73. Sim[otilde]es, LC, Sim[otilde]es, M and Vieira, MJ. 2007. Biofilm interactions between distinct bacterial genera isolated from drinking water. Appl Environ Microbiol, 73: 6192-6200.
74. Sim[otilde]es, LC, Sim[otilde]es, M and Vieira, MJ. 2010a. Adhesion and biofilm formation on polystyrene by drinking water-isolated bacteria. Antonie van Leeuwenhoek, 98: 317-329.
75. Sim[otilde]es, LC, Sim[otilde]es, M and Vieira, MJ. 2010b. Influence of the diversity of bacterial isolates from drinking water on resistance of biofilms to disinfection. Appl Environ Microbiol, 76: 6673-6679.
76. Sim[otilde]es, LC, Sim[otilde]es, M and Vieira, MJ. 2011b. The effects of metabolite molecules produced by drinking water-isolated bacteria on their single and multispecies biofilms. Biofouling, 27: 685-699.
77. Sim[otilde]es, LC, Lemos, M, Pereira, AM, Abreu, AC, Saavedra, MJ and Sim[otilde]es, M. 2011a. Persister cells in a biofilm treated with a biocide. Biofouling, 27: 403-411.
78. Sim[otilde]es, M. 2011. Antimicrobial strategies effective against infectious bacterial biofilms. Curr Med Chem, 18: 2129-2145.
79. Sim[otilde]es, M, Pereira, MO and Vieira, MJ. 2003. Effect of different concentrations of ortho-phthalaldehyde on biofilms formed by Pseudomonas fluorescens under different flow conditions. Biofouling, 19: 287-295.
80. Sim[otilde]es, M, Pereira, MO and Vieira, MJ. 2005. Action of a cationic surfactant on the activity and removal of bacterial biofilms formed under different flow regimes. Water Res, 39: 478-486.
81. Sim[otilde]es, M, Bennett, RN and Rosa, EA. 2009. Understanding antimicrobial activities of phytochemicals against multidrug resistant bacteria and biofilm. Nat Prod Rep, 26: 746-757.
82. Sim[otilde]es, M, Rocha, S, Coimbra, MA and Vieira, MJ. 2008a. Enhancement of Escherichia coli and Staphylococcus aureus antibiotic susceptibility using sesquiterpenoids. Med Chem, 4: 616-623.
83. Sim[otilde]es, M, Sim[otilde]es, LC, Machado I, Pereira, MO and Vieira, MJ. 2006. Control of flow-generated biofilms with surfactants: evidence of resistance and recovery. Food Bioprod Process, 84: 338-345.
84. Sim[otilde]es, M, Sim[otilde]es, LC, Cleto, S, Pereira, MO and Vieira, MJ. 2008b. The effects of a biocide and a surfactant on the detachment of Pseudomonas fluorescens from glass surfaces. Int J Food Microbiol, 121: 335-341.
85. Singh, BN, Singh, BR, Singh, RL, Prakash, D, Dhakarec, R, Upadhyay, G and Singh, HB. 2009. Oxidative DNA damage protective activity, antioxidant and anti-quorum sensing potentials of Moringa oleifera. Food Chem Toxicol, 47: 1109-1116.
86. Soobrattee, MA, Neergheen, VS, Luximon-Ramma, A, Aruoma, OI and Bahorun, T. 2005. Phenolics as potential antioxidant therapeutic agents: mechanism and actions. Mutat Res, 579: 200-213.
87. Srinivasan, M, Sudheer, AR and Menon, VP. 2007. Ferulic acid: therapeutic potential through its antioxidant property. J Clin Biochem Nutr, 40: 92-100.
88. Stalikas, CD. 2007. Extraction, separation, and detection methods for phenolic acids and flavonoids. J Sep Sci, 30: 3268-3295.
89. Stepanović, S, Vuković, D, Dakić I, Savić, B and Švabić-Vlahović, M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Meth, 40: 175-179.
90. Stewart, PS and Costerton, JW. 2001. Antibiotic resistance of bacteria in biofilms. Lancet, 358: 135-138.
91. Stickland, HG, Davenport, PW, Lilley, KS, Griffin, JL and Welch, M. 2010. Mutation of nfxB causes global changes in the physiology and metabolism of Pseudomonas aeruginosa. J Proteome Res, 9: 2957-2967.
92. Swamy, KCK, Kumar, NNB, Balaraman, E and Kumar, KVPP. 2009. Mitsunobu and related reactions: advances and applications. Chem Rev, 109: 2551-2651.
93. Tegos, G, Stermitz, F, Lomovskaya, O and Lewis, K. 2002. Multidrug inhibitors uncover remarkable activity of plant antimicrobials. Antimicrob Agents Chemother, 46: 3133-3141.
94. Tsompanidou, E, Sibbald, MJJB, Chlebowicz, MA, Dreisbach, A, Back, JW, Van Dijl, JM, Buist, G and Denham, EL. 2011. Requirement of the agr locus for colony spreading of Staphylococcus aureus. J Bacteriol, 193: 1267-1272.
95. Van Oss, CJ, Chaudhury, MK and Good, RJ. 1987. Monopolar surfaces. Adv Colloid Interface Sci, 28: 35-64.
96. Van Oss, CJ, Good, RJ and Chaudhury, MK. 1988. Additive and nonadditive surface tension components and the interpretation of contact angles. Langmuir, 4: 884-891.
97. Van Oss, CJ, Ju, L, Chaudhury, MK and Good, RJ. 1989. Estimation of the polar parameters of the surface tension of liquids by contact angle measurements on gels. J Colloid Interface Sci, 128: 313-319.
98. Verstraeten, N, Braeken, K, Debkumari, B, Fauvart, M, Fransaer, J, Vermant, J and Michiels, J. 2008. Living on a surface: swarming and biofilm formation. Trends Microbiol, 16: 496-506.
99. Walsh, C. 2000. Molecular mechanisms that confer antibacterial drug resistance. Nature, 406: 775-781.
100. Webster, DC, Chisholm, BJ and Stafslien, SJ. 2007. Mini-review: combinatorial approaches for the design of novel coating systems. Biofouling, 23: 179-192.
101. Xiao, J, Zuo, Y, Liu, Y, Li, J, Hao, Y and Zhou, X. 2007. Effects of Nidus vespae extract and chemical fractions on glucosyltransferases, adherence and biofilm formation of Streptococcus mutans. Arch Oral Biol, 52: 869-875.