Evaluation of the role of substrate and albumin on Pseudomonas aeruginosa biofilm morphology through FESEM and FTIR studies on polymeric biomaterials

Progress in Biomaterials

Volumn 6, Issue 1-2, 2017, Pages 27-38

  Dutta Sinha, S ^a   Chatterjee, Susmita ^b   Maiti, P K ^b   Tarafdar, S ^a   Moulik, S P ^a  

^a JADAVPUR UNIVERSITY   (India)

^b INSTITUTE OF POST GRADUATE MEDICAL EDUCATION AND RESEARCH   (India)

Author keywords

Adsorption; Bacteria; Biofilms; Biomaterials; Conditioning layer; Proteins

Indexed keywords

BACTERIAL POLYSACCHARIDE; BIOMATERIAL; BOVINE SERUM ALBUMIN; POLYETHYLENE; POLYPROPYLENE;

ARTICLE; BACTERIUM ADHERENCE; BACTERIUM ISOLATION; BIOFILM; CONTROLLED STUDY; DEVICE INFECTION; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; GENERAL MEDICAL DEVICE; IMPLANT; INDWELLING CATHETER; INFRARED SPECTROSCOPY; INTRAVENOUS CATHETER; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; SCANNING ELECTRON MICROSCOPE; URINARY CATHETER; URINARY TRACT INFECTION;

EID: 85028539509     PISSN: 21940509     EISSN: 21940517     Source Type: Journal    
DOI: 10.1007/s40204-017-0061-2     Document Type: Article

References (82)

1. Alava T, Mann JA, Théodore C, Benitez JJ, Dichtel WR, Parpia JM, Craighead HG (2013) Control of the graphene–protein interface is required to preserve adsorbed protein function. Anal Chem 85(5):2754–2759
2. Almaguer-Flores A, Olivares-Navarrete R, Wieland M, Ximénez-Fyvie LA, Schwartz Z, Boyan BD (2012) Influence of topography and hydrophilicity on initial oral biofilm formation on microstructured titanium surfaces in vitro. Clin Oral Implant Res 23(3):301–307
3. Alpkvist E, Picioreanu C, van Loosdrecht M, Heyden A (2006) Three-dimensional biofilm model with individual cells and continuum EPS matrix. Biotechnol Bioeng 94(5):961–979. doi:10.1002/bit.20917
4. Amiji M, Park K (1993) Surface modification of polymeric biomaterials with poly(ethylene oxide), albumin, and heparin for reduced thrombogenicity. J Biomater Sci Polym Ed 4(3):217–234. doi:10.1163/156856293X00537
5. An YH, Friedman RJ (1998) Concise review of mechanisms of bacterial adhesion to biomaterial surfaces. J Biomed Mater Res 43(3):338–348
6. Badihi Hauslich L, Sela MN, Steinberg D, Rosen G, Kohavi D (2013) The adhesion of oral bacteria to modified titanium surfaces: role of plasma proteins and electrostatic forces. Clin Oral Implant Res 24(A100):49–56. doi:10.1111/j.1600-0501.2011.02364.x
7. Baier RE (2006) Surface behaviour of biomaterials: the theta surface for biocompatibility. J Mater Sci Mater Med 17(11):1057–1062. doi:10.1007/s10856-006-0444-8
8. Bakker DP, Klijnstra JW, Busscher HJ, van der Mei HC (2003) The effect of dissolved organic carbon on bacterial adhesion to conditioning films adsorbed on glass from natural seawater collected during different seasons. Biofouling 19(6):391–407
9. Beal R, Betts WB (2000) Role of rhamnolipid biosurfactants in the uptake and mineralization of hexadecane in Pseudomonas aeruginosa. J Appl Microbiol 89(1):158–168
10. Beyenal H, Lewandowski Z (2000) Combined effect of substrate concentration and flow velocity on effective diffusivity in biofilms. Water Res 34(2):528–538
11. Bhosle NB, Garg A, Fernandes L, Citon P (2005) Dynamics of amino acids in the conditioning film developed on glass panels immersed in the surface seawaters of Dona Paula Bay. Biofouling 21(2):99–107. doi:10.1080/08927010500097821
12. Boulmedais F, Frisch B, Etienne O, Lavalle P, Picart C, Ogier J et al (2004) Polyelectrolyte multilayer films with pegylated polypeptides as a new type of anti-microbial protection for biomaterials. Biomaterials 25(11):2003–2011
13. Bowden GHW, Li YH (1997) Nutritional influences on biofilm development. Adv Dent Res 11(1):81–99
14. Branda SS, Vik Å, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13(1):20–26. doi:10.1016/j.tim.2004.11.006
15. Caiazza NC, Shanks RM, O’Toole GA (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187(21):7351–7361
16. Campa M, Bendinelli M, Friedman H (eds) (2012) Pseudomonas aeruginosa as an opportunistic pathogen. Springer Science & Business Media, Berlin
17. Carvalho I, Henriques M, Carvalho S (2013) New strategies to fight bacterial adhesion. In: Microbial Pathogens and Strategies for Combating them: Science, Technology and Education, Formatex Research Center, p 170–178
18. Castner DG, Ratner BD (2002) Biomedical surface science: foundations to frontiers. Surf Sci 500(1):28–60. doi:10.1016/S0039-6028(01)01587-4
19. Chae KJ, Choi MJ, Lee JW, Kim KY, Kim IS (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Bioresour Technol 100(14):3518–3525
20. Chang CC, Merritt K (1992) Microbial adherence on poly(methyl methacrylate) (PMMA) surfaces. J Biomed Mater Res 26(2):197–207
21. Chu PK, Chen JY, Wang LP, Huang N (2002) Plasma-surface modification of biomaterials. Mater Sci Eng R Rep 36(5):143–206
22. Compere C, Bellon-Fontaine MN, Bertrand P, Costa D, Marcus P, Poleunis C, Pradier CM, Rondot B, Walls MG (2001) Kinetics of conditioning layer formation on stainless steel immersed in seawater. Biofouling 17(2):129–145
23. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322
24. Dang H, Lovell CR (2016) Microbial surface colonization and biofilm development in marine environments. Microbiol Mol Biol Rev 80(1):91–138. doi:10.1128/MMBR.00037-15
25. de Paz LEC, Bergenholtz G, Svensäter G (2010) The effects of antimicrobials on endodontic biofilm bacteria. J Endod 36(1):70–77
26. del Prado G, Ruiz V, Naves P, Rodríguez-Cerrato V, Soriano F, del Carmen PM (2010) Biofilm formation by Streptococcus pneumoniae strains and effects of human serum albumin, ibuprofen, N-acetyl-l-cysteine, amoxicillin, erythromycin, and levofloxacin. Diagn Microbiol Infect Dis 67(4):311–318. doi:10.1016/j.diagmicrobio.2010.03.016
27. Dewez JL, Doren A, Schneider YJ, Rouxhet PG (1999) Competitive adsorption of proteins: key of the relationship between substratum surface properties and adhesion of epithelial cells. Biomaterials 20(6):547–559. doi:10.1016/S0142-9612(98)00207-5
28. Donlan RM (2001) Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis 33(8):1387–1392. doi:10.1086/322972
29. Etienne O, Gasnier C, Taddei C, Voegel JC, Aunis D, Schaaf P et al (2005) Antifungal coating by biofunctionalized polyelectrolyte multilayered films. Biomaterials 26(33):6704–6712
30. Falkinham JO III, Hilborn ED, Arduino MJ, Pruden A, Edwards MA (2015) Epidemiology and ecology of opportunistic premise plumbing pathogens: Legionella pneumophila, Mycobacterium avium, and Pseudomonas aeruginosa. Environ Health Perspect 123(8):749. doi:10.1289/ehp.1408692
31. Fattinger C (2014) Focal molography: coherent microscopic detection of biomolecular interaction. Phys Rev X 4(3):031024
32. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633. doi:10.1038/nrmicro2415
33. Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J Bacteriol 189(22):7945–7947. doi:10.1128/JB.00858-07
34. Foster TJ (2005) Immune evasion by staphylococci. Nat Rev Microbiol 3(12):948–958. doi:10.1038/nrmicro128
35. Freeman C, Lock MA (1995) The biofilm polysaccharide matrix: a buffer against changing organic substrate supply? Limnol Oceanogr 40(2):273–278
36. Garrett TR, Bhakoo M, Zhang Z (2008) Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 18(9):1049–1056. doi:10.1016/j.pnsc.2008.04.001
37. Haggag WM (2010) The role of biofilm exopolysaccharides on biocontrol of plant diseases. In: Elnashar M (ed) Biopolymers, InTech, Rijeka, Croatia, p 271–284, ISBN: 978-953-307-109-1
38. Hetrick EM, Schoenfisch MH (2006) Reducing implant-related infections: active release strategies. Chem Soc Rev 35(9):780–789. doi:10.1039/b515219b
39. Hochbaum AI, Kolodkin-Gal I, Foulston L, Kolter R, Aizenberg J, Losick R (2011) Inhibitory effects of d-amino acids on Staphylococcus aureus biofilm development. J Bacteriol 193(20):5616–5622
40. Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35(4):322–332. doi:10.1016/j.ijantimicag.2009.12.011
41. Hori K, Matsumoto S (2010) Bacterial adhesion: from mechanism to control. Biochem Eng J 48(3):424–434. doi:10.1016/j.bej.2009.11.014
42. Hornef MW, Wick MJ, Rhen M, Normark S (2002) Bacterial strategies for overcoming host innate and adaptive immune responses. Nat Immunol 3(11):1033–1040. doi:10.1038/ni1102-1033
43. Huang Y, Leobandung W, Foss A, Peppas NA (2000) Molecular aspects of muco-and bioadhesion: tethered structures and site-specific surfaces. J Controlled Release 65(1):63–71
44. Ignatova M, Voccia S, Gilbert B, Markova N, Cossement D, Gouttebaron R et al (2006) Combination of electrografting and atom-transfer radical polymerization for making the stainless steel surface antibacterial and protein antiadhesive. Langmuir 22(1):255–262
45. Imamura K, Shimomura M, Nagai S, Akamatsu M, Nakanishi K (2008) Adsorption characteristics of various proteins to a titanium surface. J Biosci Bioeng 106(3):273–278
46. Jiao Y, Cody GD, Harding AK, Wilmes P, Schrenk M, Wheeler KE et al (2010) Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl Environ Microbiol 76(9):2916–2922. doi:10.1128/AEM.02289-09
47. Kiehn TE, Armstrong D (1990) Changes in the spectrum of organisms causing bacteremia and fungemia in immunocompromised patients due to venous access devices. Eur J Clin Microbiol Infect Dis 9(12):869–872. doi:10.1007/BF01967501
48. Kohnen W, Kolbenschlag C, Teske-Keiser S, Jansen B (2003) Development of a long-lasting ventricular catheter impregnated with a combination of antibiotics. Biomaterials 24(26):4865–4869
49. Kugaprasatham S, Nagaoka H, Ohgaki S (1992) Effect of turbulence on nitrifying biofilms at non-limiting substrate conditions. Water Res 26(12):1629–1638
50. Lee B, Haagensen JA, Ciofu O, Andersen JB, Høiby N, Molin S (2005) Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis. J Clin Microbiol 43(10):5247–5255
51. Leonard EF, Vroman L (1992) Is the Vroman effect of importance in the interaction of blood with artificial materials? J Biomater Sci Polym Ed 3(1):95–107. doi:10.1163/156856292X00105
52. Li Z, Lee D, Sheng X, Cohen RE, Rubner MF (2006) Two-level antibacterial coating with both release-killing and contact-killing capabilities. Langmuir 22(24):9820–9823
53. Li G, Brown PJ, Tang JX, Xu J, Quardokus EM, Fuqua C, Brun YV (2012) Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol Microbiol 83(1):41–51. doi:10.1111/j.1365-2958.2011.07909.x
54. Liu J, Fu S, Yuan B, Li Y, Deng Z (2010) Toward a universal “adhesive nanosheet” for the assembly of multiple nanoparticles based on a protein-induced reduction/decoration of graphene oxide. J Am Chem Soc 132(21):7279–7281. doi:10.1021/ja100938r
55. Lynch AS, Robertson GT (2008) Bacterial and fungal biofilm infections. Annu Rev Med 59:415–428. doi:10.1146/annurev.med.59.110106.132000
56. Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39. doi:10.1016/S0966-842X(00)01913-2
57. Nakanishi K, Sakiyama T, Imamura K (2001) On the adsorption of proteins on solid surfaces, a common but very complicated phenomenon. J Biosci Bioeng 91(3):233–244. doi:10.1016/S1389-1723(01)80127-4
58. Oberhardt MA, Puchałka J, Fryer KE, Dos Santos VA, Papin JA (2008) Genome-scale metabolic network analysis of the opportunistic pathogen Pseudomonas aeruginosa PAO1. J Bacteriol 190(8):2790–2803. doi:10.1128/JB.01583-07
59. Peyton BM (1996) Effects of shear stress and substrate loading rate on Pseudomonas aeruginosa biofilm thickness and density. Water Res 30(1):29–36
60. Rios PF, Dodiuk H, Kenig S, McCarthy S, Dotan A (2007) The effect of polymer surface on the wetting and adhesion of liquid systems. J Adhes Sci Technol 21(3–4):227–241
61. Roy-Burman A, Savel RH, Racine S, Swanson BL, Revadigar NS, Fujimoto J, Sawa T, Frank DW, Wiener-Kronish JP (2001) Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis 183(12):1767–1774. doi:10.1086/320737
62. Rudra JS, Dave K, Haynie DT (2006) Antimicrobial polypeptide multilayer nanocoatings. J Biomater Sci Polym Ed 17(11):1301–1315
63. Salta M, Wharton JA, Blache Y, Stokes KR, Briand JF (2013) Marine biofilms on artificial surfaces: structure and dynamics. Environ Microbiol 15(11):2879–2893. doi:10.1111/1462-2920.12186
64. Saygun O, Agalar C, Aydinuraz K, Agalar F, Daphan C, Saygun M (2006) Gold and gold-palladium coated polypropylene grafts in a S. epidermidis wound infection model. J Surg Res 131(1):73–79
65. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. The Lancet 358(9276):135–138. doi:10.1016/S0140-6736(01)05321-1
66. Stoodley P, Boyle JD, Dodds I, Lappin-Scott HM (1997) Consensus model of biofilm structure. In: Wimpenny JWT, Handley PS, Gilbert P, Lappin-Scott HM, Jones M (eds) Biofilms: community interactions and controls, BioLine, Cardiff, U.K, p 1–9
67. Tang CJ, Zheng P, Hu BL, Chen JW, Wang CH (2010) Influence of substrates on nitrogen removal performance and microbiology of anaerobic ammonium oxidation by operating two UASB reactors fed with different substrate levels. J Hazard Mater 181(1):19–26
68. Tiller JC, Lee SB, Lewis K, Klibanov AM (2002) Polymer surfaces derivatized with poly(vinyl-N-hexylpyridinium) kill airborne and waterborne bacteria. Biotechnol Bioeng 79(4):465–471
69. Tuson HH, Weibel DB (2013) Bacteria–surface interactions. Soft Matter 9(17):4368–4380. doi:10.1039/C3SM27705D
70. van Oss CJ (1997) Hydrophobicity and hydrophilicity of biosurfaces. Curr Opin Colloid Interface Sci 2(5):503–512. doi:10.1016/S1359-0294(97)80099-4
71. van Oss CJ, Good BJ (1991) Surface enthalpy and entropy and the physico-chemical nature of hydrophobic and hydrophilic interactions. J Dispers Sci Technol 12(3–4):273–287. doi:10.1080/01932699108913130
72. Vo-Dinh T (ed) (2014) Biomedical photonics handbook: biomedical diagnostics. CRC Press, Boca Raton
73. Vogler EA (2012) Protein adsorption in three dimensions. Biomaterials 33(5):1201–1237. doi:10.1016/j.biomaterials.2011.10.059
74. von Eiff C, Jansen B, Kohnen W, Becker K (2005) Infections associated with medical devices. Drugs 65(2):179–214
75. Vu B, Chen M, Crawford RJ, Ivanova EP (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules 14(7):2535–2554. doi:10.3390/molecules14072535
76. Waldvogel FA, Bisno AL (2000) Infections associated with indwelling medical devices, 3rd edn. ASM Press, Washington DC
77. Weinstein RA, Darouiche RO (2001) Device-associated infections: a macroproblem that starts with microadherence. Clin Infect Dis 33(9):1567–1572. doi:10.1086/323130
78. Whiteley M, Bangera MG, Bumgarner RE, Parsek MR, Teitzel GM, Lory S, Greenberg EP (2001) Gene expression in Pseudomonas aeruginosa biofilms. Nature 413(6858):860–864. doi:10.1038/3510162
79. Wimpenny JW, Colasanti R (1997) A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models. FEMS Microbiol Ecol 22(1):1–16
80. Wingender J, Neu TR, Flemming HC (eds) (2012) Microbial extracellular polymeric substances: characterization, structure and function. Springer Science & Business Media, Berlin
81. Zhang X, Bishop PL, Kinkle BK (1999) Comparison of extraction methods for quantifying extracellular polymers in biofilms. Water Sci Technol 39(7):211–218
82. Zhu X, Suidan MT, Pruden A, Yang C, Alonso C, Kim BJ, Kim BR (2004) Effect of substrate Henry’s constant on biofilter performance. J Air Waste Manag Assoc 54(4):409–418