Surface roughness mediated adhesion forces between borosilicate glass and gram-positive bacteria

Langmuir

Volumn 30, Issue 31, 2014, Pages 9466-9476

  Preedy, Emily ^a   Perni, Stefano ^a,c   Nipiĉ, Damijan ^d   Bohinc, Klemen ^d   Prokopovich, Polina ^a,b,c  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c Massachusetts Institute of Technology   (United States)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; ATOMIC FORCE MICROSCOPY; BOROSILICATE GLASS; CELL ADHESION; HYDROPHILICITY; NEURAL PROSTHESES; SURFACE ROUGHNESS;

BACTERIAL ADHESION; BIOMEDICAL DEVICES; BOVINE SERUM ALBUMINS; GRAM-POSITIVE BACTERIUM; MICROBIAL ADHESION; ORTHOPEDIC DEVICES; SURFACE ASPERITIES; SURFACE CHARACTERISTICS;

BACTERIA;

BORON DERIVATIVE; BOVINE SERUM ALBUMIN; GLASS; SILICATE;

ANIMAL; BACTERIUM ADHERENCE; BOVINE; CHEMISTRY; PARTICLE SIZE; STREPTOCOCCACEAE; STREPTOCOCCUS; SURFACE PROPERTY;

ANIMALS; BACTERIAL ADHESION; BORON COMPOUNDS; CATTLE; GLASS; PARTICLE SIZE; SERUM ALBUMIN, BOVINE; SILICATES; STREPTOCOCCACEAE; STREPTOCOCCUS; SURFACE PROPERTIES;

EID: 84905967321     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la501711t     Document Type: Article

References (61)

1. Bos, R.; Van Der Mei, H. C.; Busscher, H. J. Physico-chemistry of Initial Microbial Adhesive Interactions-Its Mechanisms and Methods for Study FEMS Microbiol. Rev. 1999, 23, 179-230
2. Busscher, H. J.; Van Der Mei, H. C. How Do Bacteria Know They Are on a Surface and Regulate Their Response to an Adhering State? PLoS Pathog. 2012, 8, e1002440
3. Muszanska, A. K.; Nejadnik, M. R.; Chen, Y.; Van Den Heuvel, E. R.; Busscher, H. J.; Van Der Mei, H. C.; Norde, W. Bacterial Adhesion Forces with Substratum Surfaces and the Susceptibility of Biofilms to Antibiotics Antimicrob. Agents Chemother. 2012, 56, 4961-4964
4. Crawford, R. J.; Webb, H. K.; Truong, V. K.; Hasan, J.; Ivanova, E. P. Surface Topographical Factors Influencing Bacterial Attachment Adv. Colloid Interface Sci. 2012, 179-182, 142-149
5. Percival, S.; Malic, S.; Cruz, H.; Williams, D. Introduction to Biofilms. In Biofilms and Veterinary Medicine; Percival, S.; Knottenbelt, D.; Cochrane, C., Eds.; Springer: Berlin, 2011.
6. Van Houdt, R.; Michiels, C. W. Role of Bacterial Cell Surface Structures in Escherichia coli Biofilm Formation Res. Microbiol. 2005, 156, 626-633
7. Hori, K.; Matsumoto, S. Bacterial Adhesion: From Mechanism to Control Biochem. Eng. J. 2010, 48, 424-434
8. Cateau, E.; Berjeaud, J.-M.; Rodier, M.-H.; Imbert, C. Fungal Biofilm Inhibition By a Component Naturally Produced by Candida Albicans Yeasts Growing as a Biofilm Int. J. Antimicrob. Agents 2008, 31, 166-170
9. Piñeres, J.; Barraza, J. Energy Barrier of Aggregates Coal Particle-Bubble Through the Extended DLVO Theory Int. J. Mineral Proc. 2011, 100, 14-20
10. Walker, J. T.; Marsh, P. D. A Review of Biofilms and their Role in Microbial Contamination of Dental Unit Water Systems (DUWS) Int. Biodeterior. Biodegrad. 2004, 54, 87-98
11. Jaglic, Z.; Červinková, D.; Vlková, H.; Michu, E.; Kunová, G.; Babák, V. Bacterial Biofilms Resist Oxidising Agents due to the Presence of Organic Matter Czech J. Food Sci. 2012, 30, 178-187
12. Shi, X.; Zhu, X. Biofilm Formation and Food Safety in Food Industries Trends Food Sci. Technol. 2009, 20, 407-413
13. Poulsen, L. V. Microbial Biofilm in Food Processing Food Sci. Technol. 1999, 32, 321-326
14. Rochex, A.; Lebeault, J. M. Effects of Nutrients on Biofilm Formation and Detachment of a Pseudomonas putida Strain Isolated From a Paper Machine Water Res. 2007, 41, 2885-2892
15. Hu, Y.; Ulstrup, J.; Zhang, J.; Molin, S.; Dupres, V. Adhesive Properties of Staphylococcus epidermidis Probed by Atomic Force Microscopy Phys. Chem. Chem. Phys. 2011, 13, 9995-10003
16. Boks, N. P.; Busscher, H. J.; Van Der Mei, H. C.; Norde, W. Bond-Strengthening in Staphylococcal Adhesion to Hydrophilic and Hydrophobic Surfaces Using Atomic Force Microscopy Langmuir 2008, 24, 12990-12994
17. Tsang, C. S. P.; Ng, H.; Mcmillan, A. S. Antifungal Susceptibility of Candida albicans Biofilms on Titanium Discs with Different Surface Roughness Clin. Oral Invest. 2007, 11, 361-368
18. Percival, S. L.; Knapp, J. S.; Wales, D. S.; Edyvean, R. G. J. The Effect of Turbulent Flow and Surface Roughness on Biofilm Formation in Drinking Water J. Ind. Microbiol. Biotechnol. 1999, 22, 152-159
19. 2+ Modification of Titanium Surfaces on Early Microbial Biofilm Formation BMC Oral Health 2011, 11, 1-9
20. Cao, T.; Tang, H.; Liang, X.; Wang, A.; Auner, G. W.; Salley, S. O.; Ng, K. Y. S. Nanoscale Investigation on Adhesion of E. coli to Surface Modified Silicone Using Atomic Force Microscopy Biotechnol. Bioeng. 2006, 94, 167-176
21. Busscher, H.; Weerkamp, A. Specific and Nonspecific Interactions in Bacterial Adhesion to Solid Substrata FEMS Microbiol. Rev. 1987, 46 (2) 165-173
22. Bendersky, M.; Davis, J. M. DLVO Interaction of Colloidal Particles with Topographically and Chemically Heterogeneous Surfaces J. Colloid Interface Sci. 2011, 353, 87-97
23. Bohinc, K.; Dražić, G.; Fink, R.; Oder, M.; Jevšnik, M.; Nipič, D.; Godič Torkar, K.; Raspor, P. Available surface dictates microbial adhesion capacity Int. J. Adhes. Adhes. 2014, 50 (1) 265-272
24. Homola, A. M.; Israelachvili, J. N.; Mcguiggan, P. M.; Gee, M. L. Fundamental Experimental Studies in Tribology: The Transition From "Interfacial" Friction of Undamaged Molecularly Smooth Surfaces to "Normal" Friction with Wear Wear 1990, 136, 65-83
25. Blau, P. J. Scale Effects in Steady-State Friction Tribol. Trans. 1991, 34, 335-342
26. Allen, S.; Davies, M. C.; Roberts, C. J.; Tendler, S. J. B.; Williams, P. M. Atomic Force Microscopy in Analytical Biotechnology Trends Biotechnol. 1997, 15, 101-105
27. Mistry, S.; Kundu, D.; Datta, S.; Basu, D. Comparison of Bioactive Glass Coated and Hydroxyapatite Coated Titanium Dental Implants in the Human Jaw Bone Aust. Dent. J. 2011, 56, 68-75
28. Sader, J. E.; Larson, I.; Mulvaney, P.; White, L. R. Method for the Calibration of Atomic Force Microscope Cantilevers Rev. Sci. Instrum. 1995, 66, 3789-3798
29. Bellon-Fontaine, M. N.; Rault, J.; Van Oss, C. J. Microbial adhesion to solvents: a novel method to determine the electron-donor/electron acceptor or Lewis acid-base properties of microbial cells Colloids Surf., B 1996, 7, 47-53
30. Perni, S.; Prokopovich, P.; Piccirillo, C.; Pratten, J. R.; Parkin, I. P.; Wilson, M. Toluidine Blue-Containing Polymers Exhibit Bactericidal Activity When Irradiated with Red Light J. Mater. Chem. 2009, 19 (17) 2715-2723
31. Perni, S.; Piccirillo, C.; Parkin, I. P.; Prokopovich, P.; Chrzanowski, W.; Parkin, I. P.; Wilson, M. The Antimicrobial Properties of Light-activated Polymers Containing Methylene Blue and Gold Nanoparticles Biomaterials 2009, 30 (1) 89-93
32. Prokopovich, P.; Perni, S. An Investigation of Microbial Adhesion to Natural and Synthetic Polysaccharide-Based Films and its Relationship with the Surface Energy Components J. Mater. Sci.: Mater. Med. 2009, 20, 195-202
33. Prokopovich, P.; Starov, V. Adhesion Models: From Single to Multiple Asperity Contacts Adv. Colloid Interface Sci. 2011, 168, 210-222
34. Busscher, H. J.; Van Der Mei, R. B. H. C. Initial Microbial Adhesion is a Determinant for the Strength of Biofilm Adhesion FEMS Microbiol Lett. 1995, 128, 229-234
35. Fletcher, M. Bacterial Biofilms and Biofouling Curr. Opin. Biotechnol. 1994, 5, 302-306
36. Hall-Stoodley, L.; Costerton, J. W.; Stoodley, P. Bacterial Biofilms: From the Natural Environment to Infectious Diseases Nat. Rev. Microbiol. 2004, 2, 95-108
37. Huang, T. T.; Sturgis, J.; Gomez, R.; Geng, T.; Bashir, R.; Bhunia, A. K.; Robinson, J. P.; Ladisch, M. R. Composite Surface for Blocking Bacterial Adsorption on Protein Biochips Biotechnol. Bioeng. 2003, 81, 618-624
38. Xu, C. P.; Boks, N. P.; de Vries, J.; Kaper, H. J.; Norde, W.; Busscher, H. J.; van der Mei, H. C. Staphylococcus aureus -Fibronectin Interactions with and without Fibronectin-Binding Proteins and Their Role in Adhesion and Desorption Appl. Environ. Microbiol. 2008, 74, 7522-7528
39. Xu, L. C.; Logan, B. E. Interaction Forces between Colloids and Protein-Coated Surfaces Measured Using an Atomic Force Microscope Environ. Sci. Technol. 2005, 39 (10) 3592-3600
40. Flemming, H. C.; Wingender, J. The Biofilm Matrix Nat. Rev. Microbiol. 2010, 8, 623-633
41. Valour, F.; Trouillet-Assant, S.; Rasigade, J.-P.; Lustig, S.; Chanard, E.; Meugnier, H.; Tigaud, S.; Vandenesch, F. O.; Etienne, J.; Ferry, T.; Laurent, F. Staphylococcus epidermidis in Orthopedic Device Infections: The Role of Bacterial Internalization in Human Osteoblasts and Biofilm Formation PLoS Pathog. 2013, 8, 1-11
42. Widmer, A. F. New Developments in Diagnosis and Treatment of Infection in Orthopedic Implants Clin. Infect. Dis. 2001, 33, S94-S106
43. Rosenthal, M. E.; Dever, L. L.; Moucha, C. S.; Chavda, K. D.; Otto, M.; Kreiswirth, B. N. Molecular Characterization of an Early Invasive Staphylococcus epidermidis Prosthetic Joint Infection Microb. Drug Resist. 2011, 17, 345-350
44. Kuyukina, M. S.; Korshunova, I. O.; Rubtsova, E. V.; Ivshina, I. B. Methods of Microorganism Immobilization for Dynamic Atomic-Force Studies (Review) Appl. Biochem. Microbiol. 2014, 50, 1-9
45. Colville, K.; Tompkins, N.; Rutenberg, A. D. Jericho, M.H. Effects of Poly(L-lysine) Substrates on Attached Escherichia coli Bacteria Langmuir 2010, 26, 2639-2644
46. Fey, P. D.; Olson, M. E. Current Concepts in Biofilm Formation of Staphylococcus epidermidis Fut. Microbiol. 2010, 5, 917-933
47. Fredheim, E. G. A.; Klingenberg, C.; Rohde, H.; Frankenberger, S.; Gaustad, P.; Flægstad, T.; Sollid, J. E. Biofilm Formation by Staphylococcus Haemolyticus J. Clin. Microbiol. 2009, 47, 1172-1180
48. Loosdrecht, M. M.; Norde, W.; Lyklema, J.; Zehnder, A. B. Hydrophobic and Electrostatic Parameters in Bacterial Adhesion Aquat. Sci. 1990, 52, 103-114
49. Gharechahi, M.; Moosavi, H.; Forghani, M. Effect of Surface Roughness and Materials Composition on Biofilm Formation J. Biomater. Nanobiotechnol. 2012, 230, 541-546
50. Verran, J.; Packer, A.; Kelly, P. J.; Whitehead, K. A. Use of the Atomic Force Microscope to determine the Strength of Bacterial Attachment to Grooved Surface Features. In Surface and Interfacial Aspects of Cell Adhesion; Carré, A.; Mittal, K. L., Eds.; VSP: Leiden, The Netherlands, 2010.
51. Waerhaug, J. Effect of Rough Surfaces Upon Gingival Tissue J. Dent. Res. 1956, 35, 323-325
52. Truong, V. K.; Lapovok, R.; Estrin, Y. S.; Rundell, S.; Wang, J. Y.; Fluke, C. J.; Crawford, R. J.; Ivanova, E. P. The Influence of Nano-Scale Surface Roughness on Bacterial Adhesion to Ultrafine-Grained Titanium Biomaterials 2010, 31, 3674-3683
53. Bakker, D. P.; Busscher, H. J.; Van Zanten, J.; De Vries, J.; Klijnstra, J. W.; Van Der Mei, H. C. Multiple Linear Regression Analysis of Bacterial Deposition to Polyurethane Coatings after Conditioning Film Formation in the Marine Environment Microbiology 2004, 150, 1779-1784
54. Taylor, R. L.; Verran, J.; Lees, G. C.; Ward, A. J. The Influence of Substratum Topography on Bacterial Adhesion to Polymethyl Methacrylate J. Mater. Sci.: Mater. Med. 1998, 9, 17-22
55. Busscher, H. J.; Norde, W.; van der Mei, H. C. Specific Molecular Recognition and Interaction Forces Nonspecific Contributions to Bacterial Appl. Environ. Microbiol. 2008, 74, 2559-2564
56. Mei, L.; Busscher, H. J.; van der Mei, H. C.; Ren, Y. Influence of Surface Roughness on Streptococcal Adhesion Forces to Composite Resins Dent. Mater. 2011, 27, 770-778
57. Van der Mei, H. C.; De Vries, J.; Busscher, H. J. Weibull Analyses of Bacterial Interaction Forces Measured Using AFM Colloids Surf., B 2010, 78, 372-375
58. Mei, L.; Busscher, H. J.; Van der Mei, H. C.; Chen, Y.; De Vries, J.; Ren, Y. Oral Bacterial Adhesion Forces to Biomaterial Surfaces Constituting the Bracket-Adhesive-Enamel Junction in Orthodontic Treatment Eur. J. Oral Sci. 2009, 117, 419-426
59. Perkins, S.; Walsh, E. J.; Deivanayagam, C. C.; Narayana, S. V.; Foster, T. J.; Höök, M. Structural Organization of the Fibrinogen-Binding Region of the Clumping Factor B MSCRAMM of Staphylococcus aureus J. Biol. Chem. 2001, 276, 44721-44728
60. Mastronicolis, S. K.; Berberi, A.; Diakogiannis, I.; Petrova, E.; Kiaki, I.; Baltzi, T.; Xenikakis, P. Alteration of the Phospho- or Neutral Lipid Content and Fatty Acid Composition in Listeria monocytogenes Due to Acid Adaptation Mechanisms for Hydrochloric, Acetic and Lactic Acids at pH 5.5 or Benzoic Acid at Neutral pH Antonie Van Leeuwenhoek 2010, 98, 307-316
61. Perni, S.; Callard Preedy, E.; Prokopovich, P. Success and Failure of Colloidal Approached in Bacterial Adhesion Adv. Colloid Interface Sci. 2014, 206, 265-274